Prediction of Egeria najas and Egeria densa occurrence in a large subtropical reservoir (Itaipu Reservoir, Brazil-Paraguay)

Aquatic Botany 83 (2005) 227–238 www.elsevier.com/locate/aquabot

Prediction of Egeria najas and Egeria densa occurrence in a large subtropical reservoir (Itaipu Reservoir, Brazil-Paraguay) Luis Mauricio Bini a,*, Sidinei Magela Thomaz b a

Departamento de Biologia Geral, ICB, Universidade Federal de Goia´s, CP 131, CEP 74001-970 Goiaˆnia, GO, Brazil b Universidade Estadual de Maringa´, Nupelia, PEA-UEM, Av. Colombo, 5790, CEP 87020-900 Maringa´, PR, Brazil

Received 3 September 2003; received in revised form 10 May 2005; accepted 7 June 2005

Abstract Incidence data of two native submerged aquatic macrophytes (Egeria najas Planch. and Egeria densa Planch.) were obtained in eight arms of a large (1350 km2) subtropical reservoir (Itaipu Binacional Reservoir, Brazil-Paraguay). Environmental variables were measured simultaneously. Two large-scale surveys in the same localities identified by a global positioning system were carried out in April 1999 (n = 235) and January 2001 (n = 230). Logistic regressions were used to test the effect of environmental variables on the likelihood of E. najas and E. densa presence or absence. The two species were found under different environmental conditions: conductivity, light attenuation coefficient (k) and fetch were, in this order, the most important environmental variables in predicting the probability of occurrence of E. najas, whereas light attenuation coefficient was the main predictor of the probability of occurrence of E. densa. Thus, both species were negatively affected by the light attenuation coefficient. However, this effect was stronger in E. densa. The small area occupied by these species may be accounted for by the permanent high turbidity of Itaipu Reservoir. Additionally, the dominance of E. najas over of E. densa can be explained by the probably higher light requirements of E. densa. In other reservoirs worldwide, with higher water transparency, the opposite is frequently true. Between 1999 and 2001, an episodic water-level drawdown (5 m) caused the disappearance of submerged vegetation.

* Corresponding author. Fax: +55 62 521 11 90. E-mail addresses: [email protected] (L.M. Bini), [email protected] (S.M. Thomaz). 0304-3770/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2005.06.010

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After water-level normalization, previous vegetation presence (in 1999) was an important predictor of the probability of occurrence of E. najas in 2001. # 2005 Elsevier B.V. All rights reserved. Keywords: Hydrocharitaceae; Reservoir; Egeria najas; Egeria densa; Logistic regression

1. Introduction Hydrocharitacean species have caused extensive problems to the multiple use of aquatic ecosystems (Wells et al., 1997; Hofstra et al., 1999 and references therein). These weed problems are more accentuated in areas where these species have been introduced (Wells and Clayton, 1991). However, native species can also restrict the multiple use of some reservoirs (Ferna´ndez et al., 1990), for instance, Egeria densa Planch. and Egeria najas Planch. are two Hydrocharitaceae native to South America that have been introduced elsewhere (Cook and Urmi-Ko¨nig, 1984). Frequently, these species are considered nuisance both in their native ranges as well as in the introduced areas (Bini et al., 1999). In Jupia´ Reservoir (Parana´ River, State of Sa˜o Paulo, Brazil), for example, growth rates of these species were found to be so high that even electric power generation is affected. Most studies on E. densa have been carried out in temperate ecosystems where this species was introduced (Haramoto and Ikusima, 1988; Nakanishi et al., 1989; Wells and Clayton, 1991; Cooke et al., 1993; De Winton and Clayton, 1996; Dutartre et al., 1999). Concerning E. najas, there are few reports regarding its impacts and also little information about its ecology (Bini et al., 1999; Thomaz et al., 1999). When compared to E. najas, negative effects of E. densa on water uses are more frequent. Both species have similar architectures (submerged and canopy forming) and their geographic distribution overlaps in South America and Europe (Cook and Urmi-Ko¨nig, 1984). In this way, the difference in the capacity for invasiveness (higher in E. densa) is an intriguing subject. In this work, incidence data of E. najas and E. densa were gathered in a large subtropical reservoir (Itaipu Reservoir, Brazil-Paraguay) to answer the following questions: (i) which environmental variables predict the occurrence of E. najas and E. densa? (ii) Are the sets of predictive variables similar for both species? (iii) Why do E. najas and E. densa differ in their invasiveness capacity?

2. Study area Itaipu Reservoir is a large (1350 km2) and deep (mean depth = 22.5 m) reservoir located in the Parana´ River, between Brazil and Paraguay (248050 S and 258330 S; 548000 W and 548370 W). The theoretical residence time is 40 days, reaching ca. 29 days in the main water body, but remaining higher in the arms. Water levels are relatively stable, fluctuating less than 1.0 m/year. However, Itaipu Reservoir water level was drawn down with approximately 5 m during this study period. We surveyed eight arms varying from mesotrophic to eutrophic according to phosphorus and nitrogen concentrations (Bini et al., 1999). Previous data obtained in a

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Table 1 Descriptive statistics (mean and standard error, S.E.) for selected limnological characteristics measured at five arms (one site per arm) in Itaipu Reservoir during 1999 and 2002 Variables

Statistics

Arms AG

SFV

PC

SFF

OCO

Turbidity (NTU)

Mean S.E.

13.80 1.44

12.25 1.66

8.12 0.94

11.13 0.79

7.79 0.84

Secchi depth (m)

Mean S.E.

0.84 0.06

0.99 0.09

1.58 0.10

1.15 0.05

1.43 0.07

Alkalinity (mg L1 CaCO3)

Mean S.E.

20.42 0.36

21.01 0.78

20.35 0.42

21.50 0.46

21.39 0.40

Nitrate mg L1

Mean S.E.

0.34 0.02

0.34 0.04

0.22 0.01

0.28 0.03

0.24 0.02

Oxygen saturation (%)

Mean S.E.

98.06 1.65

105.20 3.72

98.94 1.47

99.31 1.97

98.81 1.21

Total P (mg L1)

Mean S.E.

0.03 0.01

0.03 0.00

0.02 0.00

0.02 0.00

0.01 0.00

pH

Mean S.E.

7.68 0.07

8.06 0.19

7.58 0.06

7.71 0.10

7.72 0.08

Conductivity (mS cm1)

Mean S.E.

50.13 0.79

51.50 0.89

48.50 0.87

50.88 0.76

50.44 0.88

Codes: AG, Arroio Guac¸u Arm; SFV, Sa˜o Francisco Verdadeiro Arm; PC, Passo Cueˆ Arm; SFF, Sa˜o Francisco Falso Arm; OCO, rio Ocoi Arm; data source, Itaipu Binacional.

long-term monitoring program in five of the arms show that turbidity is high and water transparency values (Secchi disk) are usually less than 2 m. Phytoplankton photosynthetic rate is high, resulting in waters with high pH and dissolved oxygen concentrations. Tributary watersheds are submitted to different land uses and impacts (e.g. farming areas, livestock inputs, domestic and industrial effluents) that may explain water characteristics variability among arms (Table 1). According to three aerial surveys and five surveys carried out by boat between 1997 and 2001, aquatic macrophytes in general and submerged vegetation in particular, are found mainly in the shallow (
3.5 m) and sheltered areas of the arms, far from the reservoir’s main channel (Thomaz et al., 1999). In these regions, littoral zones are dominated by the emergent species Urochloa plantaginea (Link) Welster and E. najas is the predominant submerged species.

3. Methods In April 1999, we surveyed eight arms of the Itaipu Reservoir. In six arms, 30 sampling sites were selected. In two small arms, sampling effort was 26 and 29 sites, in the Arroio Guac¸u and Pinto arms, respectively. In all sites (n = 235), data on E. najas and E. densa presence–absence were collected from a boat moving at low and constant velocity. A

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100 m long transect paralleling shoreline was examined at each site. We raked over the bottom to retrieve submerged species. Surveys were carried out in regions
4 m deep. At Itaipu Reservoir, submerged vegetation including the genus Egeria rarely occurs in deep waters (maximum colonization depth = 3.5 m). Thus, the majority of potential Egeria habitats within examined sites were explored. Geographical coordinates (longitude and latitude) of each site were recorded with a GPS. Some potential predictors of Egeria occurrence were also measured during the survey. Transparency was measured as Secchi depth (m). An estimate of vertical light attenuation (k in m1) was obtained by taking at least two paired measures of underwater photosynthetically active radiation (PAR) at subsurface and 0.2 m, using a Li-Cor1 underwater PAR meter. Water turbidity (NTU) and electrical conductivity (mS cm1) were recorded in the field with portable meters (LaMote-20081 and Digimed1, respectively). These variables were measured outside stands to avoid the influence of plant metabolism on water characteristics (Duarte and Kalff, 1990). For each site, the potential role of wind (‘‘wave disturbance’’) was assessed using the effective fetch (not corrected for wind speed), which was estimated by summing distances for azimuths of 0, 10, 20, . . ., 1708. The distance from each site to the main water body of the reservoir was estimated by measuring the distance from this site to the limit between the arm and the main axis of the reservoir. This limit was considered as a straight line connecting the shorelines of each arm. Finally, aquatic macrophytes species richness (minus the target species) was also used as explanatory variable in the logistic models described below. In August 1999, Itaipu Reservoir was drawn down with about 0.8–1.0 m. Later, in January 2000, the historical mean water level (225 m.a.s.l.) dropped by 5 m. The return to a more regular water-level regime (long-term mean and variation) occurred in the beginning of April 2000. The low water level during August 1999 and April 2000 reduced the area covered by submerged vegetation. This rare event was an unambiguous opportunity to evaluate the effects of this type of management in a large system like Itaipu Reservoir. In order to investigate such effects, a second survey was conducted in January 2001 using the same sampling protocol described above. Navigation to each sampling site was accomplished with a GPS. Nearly, all sites were revisited (n = 230). Between March 1997 and February 2001, variation in light attenuation coefficient was monitored in three arms (one site per arm), always at the same depth. These data were important to show the underwater light regime where plants were growing. 3.1. Data analysis The relationship between occurrence of E. densa and E. najas and environmental variables was assessed using logistic regression (Ter Braak and Looman, 1986). For each species and survey, the best combination of predictor variables was chosen using a procedure described by Wiser et al. (1998), where: (i) all predictors were tested separately; (ii) the one that results in the largest change of deviance given the degrees of freedom (assessed by the chi-square statistic) is added to the model; (iii) the procedure is repeated with all remaining predictors until addition of another variable does not result in a

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significant (at the 0.05 level) reduction in deviance (difference between chi-square statistics calculated for models with different number of predictors; see also Peeters and Gardeniers, 1998). Logistic regression model is the best choice to analyze our data set due to the characteristics of the dependent variables (binary or presence–absence of E. najas and E. densa), which were regressed on explanatory (quantitative) variables (e.g. k, fetch). Technical details and suitability of this technique to study the relationship between aquatic macrophytes occurrence (with presence–absence data) and environmental predictors can be found elsewhere (Scheffer et al., 1992; Rea et al., 1998; Van den Berg et al., 1999; Buchan and Padilla, 2000). Separate logistic regression models were estimated for each survey (April 1999 and January 2001). Similar explanatory variables were tested in both models. In 2001, the past presence of E. najas (data obtained in 1999) was included as an additional explanatory variable. Thus, because the same sites were surveyed in both years, it was possible to assess the effect of pre-existing vegetation on the presence or absence of E. najas after drawdown. Model predictive capability was evaluated by the percentage of cases in which observed data were misclassified, including both false positive and negative misclassifications. An arbitrary logit value (0.5) was used as a threshold to categorize misclassification (but see Buchan and Padilla, 2000).

4. Results 4.1. Response curves for E. najas Correlation coefficients (Pearson) among environmental variables for 1999 data were similar to correlations obtained from data collected in 2001. Only variables related to underwater light (turbidity, Secchi depth and k) were strongly correlated. For example, the lowest correlation was estimated between Secchi depth and turbidity (r = 0.64; n = 235; P < 0.001) and the highest correlation was estimated between k and turbidity (r = 0.94; n = 230; P < 0.001). Thus, to avoid multicollinearity problems involving these three variables, only k values were included in the logistic regression models. The light attenuation coefficient (k) was preferred because this variable best expressed the underwater radiation that limits primary productivity. Also, k covers attenuation by both particulate and dissolved material (the last not considered by turbidity) and is not affected by visual errors (like Secchi disk). Time series of k values obtained in three arms indicated that submerged plants grow predominantly under high turbidity (Fig. 1). According to the reduction in the deviance statistic (D), electrical conductivity (D = 5.9; P < 0.001), k (D = 3.7; P = 0.009), fetch (D = 2.9; P = 0.008) and species richness (D = 1.4; P = 0.041) were all significant predictors of E. najas occurrence, for the 1999 data set. The estimated parameter for distance from main channel was not significantly different from zero (D = 0.0; P = 0.832). It was not possible to include quadratic terms to evaluate Gaussian responses due to problems of multicollinearity generated by that inclusion. Thus, we assumed that response curves were sigmoidal.

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Fig. 1. Temporal variation in light attenuation coefficient (k) in three arms of Itaipu Reservoir, which are colonized by: Egeria SFF, Sa˜o Francisco Falso; OCO, Ocoı´; SFV, Sa˜o Francisco Verdadeiro).

For E. najas, the best model (minimal adequate model) to predict the probability of occurrence in a site included the following predictors: electrical conductivity, fetch and k. The resulting equation was: PE: na jas ¼

exp ð2:353 þ 0:067 conductivity  0:706k  0:135 fetchÞ 1 þ exp ð2:353 þ 0:067 conductivity  0:706k  0:135 fetchÞ

where PE. najas is the probability of E. najas occurrence. Comparative goodness-of-fit analysis of the different models indicated that, in fact, the successive addition of electrical conductivity (P < 0.001), fetch (P = 0.002), k (P = 0.030) resulted in a significant reduction in deviance. Reduction in deviance was not significant after the inclusion of local species richness in the model (P = 0.315). Using the variables incorporated in the minimal adequate model, sites without E. najas were predicted correctly in 81% of the cases. However, presence of E. najas was correctly predicted in only 48% of the cases. After the reservoir water-level drawdown (January 2001), E. najas occurred in only 15 sites and colonization was detected in only one site. In other words, there was a strong decrease in the spatial distribution of E. najas and a low local turnover between 1999 and 2001. In 2001, the occurrence of E. najas was significantly and negatively related to fetch (D = 5.6; P = 0.039). On the other hand, distance from main channel (D = 3.8; P = 0.045), conductivity (D = 8.6; P = 0.002), species richness (D = 21.1; P < 0.001) and E. najas occurrence in 1999 (D = 20.3; P < 0.001) were positively related to the occurrence of E. najas in 2001. However, only species richness and previous E. najas presence were significant according to the analysis of deviance (P < 0.001 for both). The minimal adequate model was: PE: na jas ¼

exp ð8:162 þ 0:763S þ 3:438 E: na jas1999 Þ 1 þ exp ð8:162 þ 0:763S þ 3:438 E: na jas1999 Þ

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where S is the species richness and E. najas1999 is the previous presence–absence of E. najas (in 1999). Using this model, sites without E. najas were predicted correctly in 99.1% of the cases. However, similarly to the data obtained in 1999, sites with E. najas were more difficult to predict and only 20% of the cases were correctly predicted. A third model was fitted to the entire data set, including data from 1999 and 2001 surveys. All significant predictors identified in the preceding minimal models were included. In addition, a dummy variable was included to allow for differences between years. In this model, all variables were significant (P-values ranging from <0.001 to 0.035) and estimated parameters presented the same signs as the previous models: PE: na jas ¼

exp ð4:28 þ 0:008 conductivity  0:38k  0:11 fetch þ 0:20S  1:85 yearÞ 1 þ exp ð4:28 þ 0:008 conductivity  0:38k  0:11 fetch þ 0:20S  1:85 yearÞ

It is important to emphasize that the significant effect of ‘‘year’’ reflected the influence of water-level drawdown on the E. najas occurrence. As in the previous models, correct predictability of E. najas absence was high (91%), while predictability of E. najas presence was low (38.1%). 4.2. Response curves for E. densa In both surveys, the spatial distribution of E. densa, as indicated by the presence across sites (12% in 1999 and 1.3% in 2001), was lower than that of E. najas (38% in 1999 and 6.5% in 2001). Light attenuation coefficient was the best predictor of the occurrence of E. densa (D = 9.3; P = 0.0018). Moreover, the occurrence of the species was significantly related to conductivity (D = 3.4; P = 0.0193) and distance from the main channel (D = 2.5; P = 0.0388). Quadratic terms were not significant. The resulting response curves were, therefore, sigmoidal. According to deviance analysis, k (P < 0.0001), conductivity (P = 0.0001) and distance from the main channel (P = 0.0002) were kept in the following multiple model: PE: densa ¼

exp ð8:02  4:14k  0:13 conductivity þ 0:23 distanceÞ 1 þ exp ð8:02  4:14k  0:13 conductivity þ 0:23 distanceÞ

Using this model, sites without E. densa were predicted more precisely than sites with E. densa (97.6 and 10%, respectively). Data obtained in 2001, for E. densa, were not analyzed by logistic regression due to the low occurrence of this species. Probability responses curves for E. najas and E. densa along environmental gradients can be used to summarize the logistic regression results (Fig. 2). The probability of E. najas occurrence is high in more sheltered sites (low fetch), with higher ionic concentrations and underwater light. The relationship between environmental predictors and occurrence of vegetation was different for the two species analyzed. For instance and most importantly, E. najas probability of occurrence was less affected by changes in k (or turbidity) than that of E.

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Fig. 2. The probability of E. najas and E. densa occurrence as a function of different environmental gradients. Only, the effects of distance from the main channel and fetch were not significant for E. najas (P = 0.8324) and E. densa (P = 0.1602), respectively. All other relationships were significant (P < 0.05). Equations of the modeled responses are shown in the text. Ranges indicated in the X-axis correspond to the observed minimum and maximum values.

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densa. Indeed, the confidence limits (99%) for the mean of k, using only values measured in the sites where E. densa was present, were 1.03 and 1.20 m1. For E. najas, the confidence limits were higher (1.20 and 1.35 m1), indicating that this species occurred at sites with higher turbidity. The occurrence of E. densa was negatively related to electrical conductivity, whereas the occurrence of E. najas was positively related to this variable. Fetch, a significant predictor of E. najas occurrence, was not included in the minimal adequate model for E. densa. The opposite was observed for the distance from the main reservoir channel, which was positively related with E. densa occurrence.

5. Discussion We found that several environmental variables were important to predict the distribution of E. najas. Considering that: (a) bicarbonate concentrations are strongly and linearly related to electrical conductivity in most types of freshwater ecosystems (Vestergaard and Sand-Jensen, 2000) and (b) considering the capacity to use bicarbonate ions in the genus Egeria (Rascio et al., 1991; Pierini and Thomaz, 2004), we infer that the relationship between the probability of E. najas occurrence and electrical conductivity may be explained by the favored growth of E. najas in waters with higher bicarbonate concentrations. Different studies showed that the growth rates of some submerged, eutrophication-tolerant, canopy forming angiosperms, collectively called elodeids, are stimulated by the increase of bicarbonate concentrations (Madsen and Sand-Jensen, 1987; Vadstrup and Madsen, 1995). On the other hand, the negative relationship between conductivity and the occurrence of E. densa is difficult to explain. Due to the scattered distribution of stands in large arms and since our water samples were collected outside stands, the influence of plant metabolism upon water characteristics was minimal. Rea et al. (1998) also reported declining probabilities of macrophyte occurrence with increasing fetch. However, a negative relationship cannot be considered a general pattern since other studies indicated enhanced abundance of submerged macrophytes at sites with higher fetches (Keddy, 1983; Scheffer et al., 1992). Positive relationships between underwater light incidence and different measures of aquatic macrophytes abundance or growth (e.g. cover, biomass, photosynthetic rate, depth of maximum colonization) have been detected often (Spence, 1982; Duarte et al., 1986; Duarte and Kalff, 1990; Madsen and Maberly, 1991; Scheffer et al., 1992; Feijoo´ et al., 1996; Schwarz et al., 2000). Tanner et al. (1993) found that E. densa, growing from a depth of 1.85 m, requires k values lower than 1.65 m1 for a positive growth rate. They suggest that at k levels above about 2 m1 establishment of E. densa would be unlikely. It is interesting to observe the similarity between this result and the results obtained in this study (Fig. 2). E. densa and E. najas are able to grow under low light conditions (Barko and Smart, 1981; Wells and Clayton, 1991; Tavecchio and Thomaz, 2003). Under these conditions, species that store enough energy in tubers and rhizomes may re-allocate resources to elongate shoots (Tanner et al., 1993; Hofstra et al., 1999). Thus, after canopy formation near the water surface, these species may have escaped the effects of turbidity (Scheffer et al., 1992). In E. densa and E. najas carbohydrates are mainly stored in the

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shoots. In this way, the escape effect, if any, should be effective only after canopy formation, in an earlier period, when irradiance levels were high enough to permit these plants to reach the water surface. Between December 1999 and February 2000 (70 consecutive days), water level had decreased by about 5 m in Itaipu Reservoir. As indicated above, E. najas colonizes regions usually shallower than 3 m. Thus, the decrease in water level of 5 m affected the entire potential area of colonization by Egeria in the reservoir. The significant reduction of E. najas occurrence in 2001 may thus be explained by the drawdown. However, the efficiency of water-level drawdown to control aquatic macrophytes is a controversial issue due to undesired side effects (see Cooke et al., 1993 and references therein). The significant relationship between E. najas occurrence in 1999 and E. najas occurrence in 2001, after water-level drawdown, may be explained by the presence of a propagule bank or by recolonization from propagules originated in other sites. In E. densa, stem fragments that contain double nodes can develop into new plants (Getsinger and Dillon, 1984). Mature seeds are rarely found in nature (Cook and Urmi-Ko¨nig, 1984). Thus, new stands are probably generated by unspecialized regenerative propagules. During periods of low water level, the cover created by the exposed vegetation may be important to sustain moisture conditions allowing the persistence of some regenerative fragments. In fact, some studies have indicated the persistence of viable propagules under dry conditions (De Winton and Clayton, 1996 and references therein). Due to the low E. najas occurrence after water-level restoration, assuming a high level of stochasticity associated with dispersal processes and the possibility of propagules that may persist under vegetation cover, it is suggested that the hypothesis of regeneration of E. najas by autochthonous fragments seems the most plausible. Despite the worldwide occurrence of E. najas (Cook and Urmi-Ko¨nig, 1984), it is still unknown why E. densa is considered the main nuisance in several parts of the word. Considering the high potential of infestation of E. densa, why is E. najas more widely distributed in the Itaipu Reservoir? Why would both species not cause nuisance in this reservoir? The results of this study suggest that different environmental requirements of these species may answer the last question. Despite canopy formation, underwater light is an important factor that restricts both species in the shallow regions of Itaipu Reservoir. However, logistic regressions indicate a stronger decrease of the probability of E. densa occurrence as a function of light attenuation coefficient (k), which is the main predictor of the occurrence of this species. Light attenuation measurements from three monitoring sites (Fig. 1) indicate that light attenuation coefficients are rarely lower than 1.5 m1 (mean = 2.6 m1; S.E. = 0.22 m1; n = 90). Thus, if a k value equal to 2 m1 is considered restrictive for Egeria growth, we suggest that light availability is generally inadequate in the Itaipu Reservoir. A higher tolerance of E. najas to turbidity (see Fig. 2) may explain the higher frequency of this species at Itaipu Reservoir. Data on maximum colonization depth of E. najas and E. densa at Itaipu Reservoir and other Brazilian reservoirs also corroborate the hypothesis of a higher tolerance of the former species to high turbidity. At Jupia´ Reservoir, where E. densa and E. najas cause strong problems, water transparency is higher (Secchi depth = 4.5 m) than at Itaipu Reservoir (1.5 m).

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Probably, high underwater light availability in temperate ecosystems and some unknown competitive advantage of E. densa under these conditions, compared to E. najas, explains the higher invasiveness of the former.

Acknowledgments We thank Dr. Adriano S. Melo (Universidade Federal do Rio Grande do Sul) for reviewing drafts of the manuscript and Hazel MacLeod (Glasgow University) for English revision. LMB and SMT are Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq) researches and acknowledge the grants from this agency. Work by LMB was also supported by Fundac¸a˜o de Amparo a` Pesquisa da Universidade Federal de Goia´s (FUNAPE/UFG). Itaipu Binacional provided funds for this study.

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