The use of indices for evaluating the periphytic community in two kinds of substrate in Imboassica Lagoon, Rio de Janeiro, Brazil

Aplicação de índices para a avaliação da comunidade perifítica em dois tipos de substrato na lagoa Imboassica, Rio de Janeiro, Brasil

The use of indices for evaluating the periphytic community in two kinds of substrate in Imboassica Lagoon, Rio de Janeiro, Brazil

Aplicação de índices para a avaliação da comunidade perifítica em dois tipos de substrato na lagoa Imboassica, Rio de Janeiro, Brasil

Fernandes, V. O.^I; Esteves, F. A.^II

^IUniversidade Federal do Espírito Santo, CCHN, Departamento de Ciências Biológicas, Setor: Botânica, Av. Marechal Campos, 1468, CEP 29060-900, Maruípe, Vitória, ES, Brazil

^IIUniversidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Ecologia, Ilha do Fundão, CEP 21541-590, Rio de Janeiro, RJ, Brazil

^{Correspondence}

ABSTRACT

Biological indices based on the biomass (dry weight, ash content, and chlorophyll-a) of the periphyton in a natural (submersed leaves of Typha domingensis Pers) and in an artificial (plastic hoses) substrate were compared, in experiments performed in summer and winter, in two sampling stations of Imboassica Lagoon, Macaé, Rio de Janeiro. The periphytic community exhibited low biomass at the beginning and end of the experiments, and moderate biomass in the intermediate period of the experiment, whatever the kind of substrate, sampling station, and season. In both seasons, there was a spatial variation regarding the degree of trophy of the periphyton, due to the difference of nutrient availability among the sampling stations. The alternation of inorganic and organic periphyton, as well as of their heterotrophic, hetero-autotrophic, auto-heterotrophic and, autotrophic character was due to changes in the abiotic factors of the sampling periods. The Lakatos index proved more sensitive than the Autotrophic Index to variations in the composition of the periphytic community.

Key words: periphyton, natural and artificial substrate, index, coastal lagoon.

RESUMO

Índices biológicos baseados na biomassa (peso seco, conteúdo de cinzas e clorofila a) do perifíton em substrato natural (folhas submersas de Typha domingensis Pers) e artificial (mangueiras plásticas) foram comparados, em experimentos realizados durante o verão e o inverno, em duas estações de amostragem da lagoa Imboassica, Macaé, Rio de Janeiro. A comunidade perifítica apresentou baixa biomassa nas fases iniciais e finais dos experimentos e biomassa média nas fases intermediárias, independente do tipo de substrato, estação de amostragem e período estudado. Em ambos os períodos, houve variação espacial com relação ao grau de trofia do perifíton em razão da diferença de disponibilidade de nutrientes entre as estações de amostragem. As alternâncias do perifíton inorgânico e orgânico, heterotrófico, hetero-autotrófico, auto-heterotrófico e autotrófico se deveram a mudanças nos fatores abióticos nas estações de amostragem nos períodos estudados. O índice de Lakatos mostrou-se mais sensível às variações na composição da comunidade perifítica do que o Indíce Autotrófico.

Palavras-chave: perifíton, substrato natural e artificial, índices, lagoa costeira.

INTRODUCTION

According to Kjerfve (1994), coastal lagoons are shallow bodies of water, found in all continents, usually parallel to the shoreline, and separated from the sea by a sandbar or connected by one or more channels. Differences in the degree of marine influence, morphometry, and extension are characteristics of Brazilian coastal lagoons especially regarding the communities inhabiting them and environmental variables (Esteves et al., 1990).

In the coastal lagoons the photic zone often reaches the sediment and, thus, submersed and floating aquatic macrophytes, as well as submersed structures of emergent macrophytes and dead substrates are densely colonized by sessile microflora (Fernandes, 1997).

The periphyton is represented by a bioderm composed of microorganisms (bacteria, fungi, algae, protozoa, and microcrustaceans), as well as organic and inorganic detritus, that may have adhered to or be associated with a substrate, living or dead (Wetzel, 1983a; Moschini-Carlos & Henry, 1997). Functionally, it is a microcosm where internal (autotrophic and heterotrophic) processes and exchanges with the external environment (surrounding water) occur simultaneously (Wetzel, 1983b). The community composition varies in relation to such diverse factors as the nature of the substrate and the trophic state of the environment (Moschini-Carlos & Henry, 1997).

In coastal lagoons subjected to anthropogenic stress, periphytic biomass growth may be explained by nutrient inputs (e.g., domestic effluent dumping) and modifications of abundance development may be controlled by opening the sandbar (Fernandes, 1997). According to Watanabe (1985), many indices based on dry weight, organic matter, and chlorophyll-a may be used for classifiying periphyton during the substrate colonization phases, according to autotrophic or heterotrophic state, organic or inorganic nature, and biomass.

The aims of this research were to classify and compare the development of the periphytic community, using different biological indices, in experiments performed with natural and artificial substrates in a Brazilian coastal lagoon.

STUDY AREA

Imboassica Lagoon is located inside the urban perimeter of Macaé, in northern Rio de Janeiro State, between 23^o25' and 23^o35'S, 42^o35' and 42^o45'W. The great surface:depth ratio is a positive characteristic for colonization of several aquatic macrophyte species, mainly Typha domingensis Pers (Furtado, 1994). The lagoon is separated from the sea by a sandbar approximately 50 meters wide. At the opposite end, where the Imboassica River reaches the lagoon, a salinity gradient between the mouth zone of the river was detected (Fernandes, 1997) (Fig. 1).

Within the last few years a great number of houses with unsuitable sewage systems have been constructed on the shores of the Imboassica Lagoon and untreated domestic sewage dumping occurs in this aquatic ecosystem.

Artificial openings of the sandbar also greatly impact this ecosystem and occur after intense rain, when flooding occurs in the shore regions and sewage effluents accumulate in the lagoon. A drastic decrease in lagoon water volume is then observed, since most of the water is drained into the sea, with the lacustrine sediment being exposed in many places and considerable loss of emergent and submersed aquatic macrophyte organisms, as well as associated periphytic communities.

MATERIALS AND METHODS

Two sampling stations were selected: station 1, in the mouth zone of the main sewage channel, and station 2, approximately 200 meters from station 1, in a region less densely colonized by aquatic macrophytes and more exposed to wind effects (Fig. 1).

The experiments were performed in summer (February and March 1994) and in winter (July and August 1994). In the summer, beginning from February 2, samples were taken after 1, 3, 5, 8, 15, 20, 24, and 32 days; in the winter, from August 2 on, the periphyton was collected after 1, 3, 5, 8, 15, 22, 29, and 35 days.

In both sampling stations, water samples collected at the subsurface (about 20 cm depth) were used for determining pH (Micronal B278 pHmeter), salinity and electrical conductivity (H-01474-00 salinometer-conductivimeter), dissolved oxygen (TOA oxymeter), and total phosphate (Golterman et al., 1978), and then filtered in Whatman GF/C filters for dissolved nutrients (amonniacal nitrogen, Koroleff, 1976; nitrate, Zagato et al., 1981; dissolved total phosphorus and total phosphate, Golterman et al., 1978). Water temperature and transparency were also measured using a FAC 400 thermistor and Secchi disk, respectively.

In each period, we selected as a natural substrate about 100 leaves of adult, green, emergent leaves (from 2.5 to 3.0 meters, at station 1, and from 1.5 to 2.0 meters, at station 2), of Typha domingensis, which were marked at the water-air interface with plastic-covered wires. They were incubated thereafter at a 20 cm depth, for periphyton colonization.

At both sampling stations, as an artificial substrate, we used plastic hoses 1.0 cm in diameter attached to a 1.5 by 0.80 m rectangular wooden frame, and fixed in the sediment.

In each sampling, periphyton samples from the natural and artificial substrates were removed and transfered in glass containing previously filtered water. The periphyton was then separated from the substrates by scraping and the substrate surface areas were determined with a pachymeter.

For the dry weight (DW) and ash-free dry weight (AFDW) periphyton determinations, the material was diluted in water and homogenized, after scrubbing. Replicates of 100 ml of the samples were vacuum filtered in pre-burned Whatman GF/C filters. Afterward, the filters were dried on a stove (at 70^oC) until a constant dry weight. They were subsequently burned for three hours using a muffle furnace (at 450^oC). The filters were weighed again and the ash-free dry weight (AFDW) was determined by the difference between the DW and the remaining weight.

From the same periphytic material, other 100 ml samples were strained with filters which had not been pre-incinerated and were immediately frozen. After, chlorophyll-a was determined according Nusch & Palme (1975) using warm ethanol (80^oC) as a solvent. For the periphyton classification, two indices were adopted:

a. The Autotrophic Index (AI), which represents the quotient between ash-free dry weight and chlorophyll-a values (Apha, 1985) used for characterizing periphytic colonization stages on substrates, and related to the trophic state of the community.

b. The index proposed by Lakatos (1989) based on chlorophyll-a (%), ashes (in % of DW), and dry biomass (g.m^–2) values, as shown in Table 1.

The sampling stations were chosen to test the hypothesis that the periphytic community would be different in stations, substrates, and seasons as a consequence of observed alterations in environmental conditions.

RESULTS

Table 2 shows the physical, chemical, and physicochemical factors in two sampling stations of Imboassica Lagoon.

In summer, water temperatures were high, ranging from 24.1^oC to 29.8^oC at station 1 and 24.1^oC to 30.5^oC at station 2. In winter, the water temperatures varied between 18.7^oC and 24.1^oC (station 1) and 17.9^oC to 24.0^oC (station 2). Generally, the transparency was high considering the total Imboassica Lagoon depth. In summer, water transparency reached the sediment in both sampling stations (from 0.80 to 1.20 m). In winter, water transparency ranged from 0.04 m (after rain) to 1.15 m at station 1 and from 0.85 m to 1.10 m at station 2.

Electrical conductivity was higher in winter than in summer, mainly at station 2. The average electrical conductivity value was 2.6 mS/cm in summer and 5.2 mS/cm in winter.

The pH results showed that Imboassica Lagoon was slightly alcaline to alcaline at both sampling stations and in both periods, with an average pH value of 7.5 at sampling station 1 and 7.6 in sampling station 2 (in summer), and pH values of 7.2 and 7.6 at sampling station 1 and 2, respectively (in winter).

The total alkalinity values were considerably higher in summer (more than twice those registered in the winter), ranging from 1.03 meq/L to 1.38 meq/L at station 1; at station 2, the variation was from 1.01 meq/L to 1.55 meq/L. In winter at station 1 the total variation ranged between 0.19 meq/L and 0.56 meq/L and at station 2, the total variation ranged from 0.15 meq/L to 0.83 meq/L.

Salinity values were higher in winter than in summer due to marine influence in the lagoon after an opening in the sandbar. Imboassica Lagoon was characterized as oligohaline to oligo-mesohaline in summer and winter, respectively.

Table 3 presents the concentrations of dissolved nutrients and total nutrients in the two sampling stations in the different samplings. In summer, as well as in winter, on most sampling days, station 1 exhibited higher nutrient concentrations when compared to station 2.

Tables 4 and 5 show the variation of periphytic biomass (based on ashes, chlorophyll-a, and dry weight values) in summer and winter, in the natural and in the artificial substrates at the sampling stations and the corresponding classification according to Lakatos (1989) and Apha (1985).

In summer, the periphytic community of the natural substrate presented low biomass at station 1 (Table 4) as it did in the first and last stages of the experiment in the artificial substrate. In station 2, the periphyton of the natural substrate presented low biomass values except on the 20^th day. In the artificial substrate, the biomass was high only from the 8^th to the 20^th day (Table 4).

In winter, the periphyton showed low biomass until the 29^th and 22^nd day of exposition of natural substrates of stations 1 and 2, respectively, increasing from then on until the final stages (Table 5). The artificial substrate of station 1 showed low biomass in the first and last stages and increased in the intermediate stages. The artificial substrate of station 2 presented low biomass up to the 22^nd day, and increased from that day on.

During the summer at station 1 the natural substrate showed organic fraction predominance in the first and final stages of the experiment, and organic-inorganic fractions occurred from the 8^th to the 15^th day. In the artificial substrate the inorganic-organic fraction predominated until the 15^th day, being replaced by the organic fraction until the end of the experiment. In station 2, the periphyton was characterized as predominantly organic until the 8^th day of exposition of the substrate (in the natural substrate) and the 5^th day (in the artificial substrate). From then on, deposition of inorganic material occurred and the periphyton was characterized as being inorganic-organic (Table 4).

In winter, independently of substrate or sampling station, there was an alternation of the inorganic-organic fractions of periphyton in both substrates and both sampling stations.

Using the percentage of chlorophyll-a to characterize the periphyton which had adhered to the natural substrate of station 1 in summer, the biomass was labeled as heterotrophic for the first few days, then characterized as heterotrophic-autotrophic until the 15^th day and, from then on, as autotrophic. The periphyton in the artificial substrate of this same sampling station presented characteristically heterotrophic initial stages; there then occurred a gradual algae colonization increase in the community, characterizing autotrophic periphyton. In summer, both the natural and artificial substrate in station 2 exhibited a community with heterotrophic characteristics throughout the experiment (Table 4).

In winter, the natural substrate of station 1 showed autotrophic periphyton from the 15^th to the 29^th day of substrate exposition during which the artificial substrate presented heterotrophic-autotrophic characteristics. In both substrates, the first and last days of the experiment exhibited more heterotrophic characteristics. In station 2, heterotrophy was dominant in both substrates in such a way that, in the natural substrate, in the intermediate stages (5^th to 22^nd day) the periphyton was characterized as heterotrophic-autotrophic; in the artificial substrate this kind of community developed only on the 15^th day of colonization (Table 5).

Tables 4 and 5 also show the fluctuations in the Autotrophic Index in the different stages of periphyton colonization in both substrates and sampling stations where, by the way, in summer and winter the periphyton was generally heterotrophic.

DISCUSSION

The differences of the abiotic factors in Imboassica Lagoon became evident in both spatial and temporal scales. The temporal heterogeneity may be explained by sandbar openings on two occasions a few months before the winter experiment. The consequent marine influence resulted in higher values of salinity and electrical conductivity.

Spatial heterogeneity was due to the variation in concentrations of ammoniacal-N and total-P, which exhibited, on most sampling days and in both periods, higher values at station 1, located in the mouth of the sewage channel.

In the rainy season a water level increase in the sewage channel occurred and nutrient input and water transparency was reduced in station 1.

Imboassica Lagoon presented fresh-to-oligohaline water, since the sandbar had been closed for 1 year and 4 months prior to the first experiment. The sandbar was then opened for a short period of time. Later, due to continued rain, the sandbar was opened again (in the beginning of May). The second experiment was, therefore, performed at a time when the lagoon exhibited mesohaline characteristics.

Thus, the experiments were developed in distinct climatic and environmental conditions which exerted some influence on the periphytic community structure and dynamics (Fernandes, 1997).

According to Moschini-Carlos (1996), the composition and abundance of periphytic algae are a result of abiotic factors, such as temperature, light, and nutrients. These organisms are, therefore, very sensitive to systemic modifications in water quality and hydrodynamics.

The periphytic algae may absorb nutrients, when available in the water column, while maintaining the internal nutrient pool which allows their development even in oligotrophic conditions (Chamixaes, 1991).

The influence of the sewage channel in station 1 and the openings of the sandbar between the studied periods were the factors that promoted marked effects in the biomass and on the periphytic community structure and dynamics in Imboassica Lagoon.

The periphyton may be characterized using indices, based on total biomass, chlorophyll-a, and ash content which allow estimating their community structure and productivity (Watanabe, 1990). The periphytic community includes autotrophic and heterotrophic organisms, as well as inorganic and organic detritus of allochthonous and autochthonous origin. According to Lakatos (1989), the periphytic biomass, estimated by the ash content, includes predominantly inorganic material and, when estimated by chlorophyll-a, corresponds to the photosynthetic algae community.

The low periphytic biomass found in the first and last stages of the experiment, in both substrate and sampling stations, may be explained by the P deficiency in the water column (in station 1), and of N and P in the water column (in station 2). Evidence that the low nutrient availability in the water column limits periphytic algae growth, has already been reported (Sand-Jansen, 1983; Chamixaes, 1991; Fernandes, 1997).

In the intermediate stages of the experiment (between the 8^th and 24^th day in summer and the 8^th and the 22^nd day in winter), the periphytic biomass presented high values due to the greater algae density and had more autotrophic characteristics, based on the chlorophyll-a values.

The temporal variation in ash and chlorophyll-a contents indicates a change from the predominantly autotrophic organisms to heterotrophic ones, or in the presence of organic or inorganic materials deposited on the substrates. Greater algae colonization in the periphytic community with, therefore, more autotrophic characteristics, is directly related to the degree of trophy of the environment.

In summer as well as in winter, autotrophic and autotrophic-heterotrophic conditions were found in the intermediate stages of the experiment in the substrates of station 1. In the natural substrate, the autotrophic stages lasted longer. This fact may possibly be explained by the "preference" of the organisms for colonizing living substrates and by the nutrient exchange between the substrate and the periphytic community. In this sampling station, algae colonization was made easier by the greater nutrient input (N and P) in the area around the sewage channel's mouth. In station 2, heterotrophy was characteristic of the periphytic community throughout almost all of the summer and winter, in the natural as well as in the artificial substrate. In this sampling station, the lower nutrient availability must have been one of the major factors controlling density algae in both substrates.

The more heterotrophic characteristics of the periphytic community must be directly related to various factors such as: greater density of bacteria and/or fungi, which are characteristically pioneering organisms in many experiments performed by several authors (Wetzel, 1983b; Godinho-Orlandi & Barbieri, 1983; Fernandes, 1993; Moschini-Carlos & Henry, 1997); low density of organisms in the first stages of colonization; loosening of periphytic organisms in the final stages; and storage in the substrates of inorganic material from the sewage channel or regions close to the lagoon, especially in periods of high precipitation. These combined factors should explain the change from organic-inorganic to inorganic-organic periphyton in both periods in the two substrates and sampling stations (Fernandes, 1997).

Using the Autotrophic Index, heterotrophy was shown to dominate in the periphytic community in both sampling stations and substrate types in Imboassica Lagoon. Only the intermediate stages of the experiment exhibited more autotrophic characteristics (from the 15^th day of colonization).

Schwarzbold (1992) and Fernandes (1993), developing similar experiments with adhered periphyton in natural substrates in the Infernão (SP) and Jacarepaguá (RJ) lagoons and using the Autotrophic Index, classified the community as having heterotrophic characteristics. Moschini-Carlos & Henry (1997), working with natural and artificial substrates in the Jurumirim Reservoir (SP) and using the Autotrophic Index and the Lakatos index as classification indices, characterized the periphyton as being heterotrophic-autotrophic.

On most days our study, the characteristics described in the Autotrophic Index coincided with those defined in the Lakatos index. The latter, however, was more sensitive to modifications in composition of the community.

Acknowledgments – The authors extend their thanks to Petrobrás for financially assisting this project. Our thanks to Paulo Roberto Brum for translating the manuscript into English.

Received Juny 10, 2002 – Accepted October 22, 2002 – Distributed May 31, 2003

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Publication Dates

• Publication in this collection
  08 Sept 2003
• Date of issue
  May 2003

History

• Accepted
  31 May 2003
• Reviewed
  22 Oct 2002
• Received
  10 June 2002