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Response of native Egeria najas Planch. and invasive Hydrilla verticillata (L.f.) Royle to altered hydroecological regime in a subtropical river
Aquatic Botany 92 (2010) 40–48
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Response of native Egeria najas Planch. and invasive Hydrilla verticillata (L.f.) Royle to altered hydroecological regime in a subtropical river Wilson Treger Z. Sousa a,*, Sidinei M. Thomaz a, Kevin J. Murphy b a b
Universidade Estadual de Maringa´, Nupe´lia, Av. Colombo 5790, 87020-900 Maringa´, Pr, Brazil Division of Ecology and Evolutionary Biology, Faculty of Biomedical and Life Sciences, University of Glasgow G12 8QQ, Scotland, UK
A R T I C L E I N F O
A B S T R A C T
Article history: Received 4 March 2009 Received in revised form 29 September 2009 Accepted 5 October 2009 Available online 12 October 2009
Egeria najas Planch. is the dominant native submersed macrophyte of the Upper Parana´ River in Brazil, while Hydrilla verticillata (L.f.) Royle has recently invaded this area. From January 2006 to December 2007, comprising two annual flood cycles, we conducted monthly surveys at two river stations and two lakes connected to the river within this stretch of the Parana´ River, aiming to understand how the hydrological regime influences the distribution and abundance of these native and invasive Hydrocharitaceae species. Hydrilla did not develop in the lakes, possibly due to the elevated proportion of organic matter in the sediment (10% DW). However, the exotic species dominated the river sites apparently suppressing E. najas. In the lakes E. najas reached a maximum biomass of 628 82 g DW m2 but did not surpass 333 83 g DW m2 in the river, where H. verticillata peaked at 1415 255 g DW m2. Macrophyte biomass development was greatest during low-water periods, with transparent water and high temperatures. Floods probably affected submersed macrophytes (especially in 2007, when an extreme flood caused by an El Nin˜o Southern Oscillation (ENSO) event occurred) via sediment movement and plant scouring (uprooting) effects, coupled with reduced water transparency. Macrophyte recovery started soon after the (less intense) 2006 flood but was delayed in 2007. In the river recovery started five months after the major flood, but in the lakes no significant plant regeneration was found even nine months after the disturbance. E. najas and H. verticillata started regeneration practically at the same time but H. verticillata had much higher rates of biomass increase. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Hydrocharitaceae Biomass Flood disturbance Regeneration Riverine floodplain ENSO
1. Introduction Hydrilla verticillata (L.f.) Royle, one of the most successful aquatic weeds in the world (Murphy, 1988; Mullin et al., 2000; Hershner and Havens, 2008), is newly invasive in the Upper Parana´ River catchment (first recorded in June 2005: Thomaz et al., 2009). Egeria najas Planch. is the dominant native submersed plant in this river and its associated floodplain waterbodies. Although it is regarded as a potential nuisance species that can cause localized problems in reservoirs (Thomaz and Bini, 1999; Martins et al., 2005, 2008), E. najas is not invasive outside its native range of southern Brazil, north east Argentina and Paraguay (Cook and Urmi-Ko¨nig, 1984). Both species are members of the family Hydrocharitaceae with very similar morphology and ecological characteristics. They grow vertically in the water column, forming
* Corresponding author. Tel.: +55 44 3261 4616. E-mail addresses: [email protected] (W.T.Z. Sousa), [email protected] (S.M. Thomaz), [email protected] (K.J. Murphy). 0304-3770/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2009.10.002
dense canopies near the water surface and show physiological plasticity which enables growth under low levels of light and inorganic carbon (Van et al., 1976; Barko and Smart, 1981; Spencer et al., 1994; Kahara and Vermaat, 2003; Tavechio and Thomaz, 2003; Pierini and Thomaz, 2004). However, unlike E. najas, H. verticillata has specialized structures for vegetative reproduction (tubers and turions) besides a well-developed rhizome system capable of stocking carbohydrate reserves which enable the plant to persist and recover quickly even after severe disturbances (Owens and Madsen, 1998; Madsen and Smith, 1999). H. verticillata can potentially displace native submersed macrophyte communities (Van et al., 1999; Mony et al., 2007; Wang et al., 2008). Since E. najas and H. verticillata display very similar ecological strategies and growth form, competitive interaction could be intense. While H. verticillata is one of the most extensively studied aquatic macrophytes, there is only scarce information about the biology and ecology of E. najas (e.g. Tavechio and Thomaz, 2003; Pierini and Thomaz, 2004), especially in its native habitats (Bini and Thomaz, 2005; Thomaz et al., 2006). Improved understanding of which factors affect the population
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dynamics of these native and exotic Hydrocharitaceae can help in the development of conservation and management plans (Murphy and Pieterse, 1990; Wingfield et al., 2006). Hydrological regime is considered the key factor driving ecological functioning and biodiversity patterns in river-floodplain systems (Junk et al., 1989; Neiff, 1990; Ward et al., 2002; Thomaz et al., 2007). Variations in water level potentially lead to significant changes in aquatic plant communities (Bornette et al., 1994; Van Geest et al., 2005; Maltchik et al., 2007; Santos and Thomaz, 2007). According to the intermediate disturbance hypothesis (Connell, 1978), hydrological disturbances tend to disrupt competitive processes among aquatic plants opening gaps for colonization and development of less competitive species (Junk et al., 1989; Bornette et al., 1994; Santos and Thomaz, 2007). For example, after flood disturbances in a former channel of the Rhoˆne River, France, Henry et al. (1996) found that the first species to reestablish were able to produce turions or other non-subterranean vegetative organs. Hence, in the Upper Parana´ River floodplain, flood disturbances could help to prevent competitive exclusion of native species by H. verticillata or conversely might accelerate exclusion processes, if the recovery rate of the exotic plant is much quicker than that of the native plants (Henry et al., 1996; BarratSegretain et al., 1998; Bornette et al., 2008). In this investigation we monitored the environmental parameters and the dynamics (biomass and height) of monospecific Hydrocharitaceae stands over 24 months in two sites of the Parana´ River and two connected lakes aiming to understand how the hydrological regime influences the distribution and abundance of E. najas and H. verticillata. The river sites and connected lakes represent two types of floodplain habitats characterized by different degrees of connectivity with the river and thus presenting different environmental characteristics such as hydrology (e.g. lotic vs. semi-lentic) and geomorphology (e.g. open vs. protected areas). The specific questions of this study are (1) is there a difference between the native and the invasive Hydrocharitaceae regarding their spatial and temporal patterns of distribution and abundance (e.g. response to flood disturbances)?; (2) is there a difference between river sites and connected lakes concerning the macrophyte dynamics (e.g. resilience to flood disturbances)?; (3) which environmental variables can best explain E. najas and H. verticillata biomass and rate of net biomass increase (NBI)? and (4) what are the effects of intra-annual (seasonal water level
41
˜ o South Oscillation variations) and inter-annual (normal vs. El Nin (ENSO) flood) on macrophytes in two categories of sites (lakes vs. river)? Our results are also of interest because during the study period we had the opportunity to assess the effects of an extreme, low recurrence flood, caused by an ENSO, which happens every 5–7 years in the Parana´ River system. 2. Materials and methods 2.1. Study area The Upper Parana´ River floodplain is the only remaining stretch (about 230 km long and up to 20 km wide) of the river inside Brazil without dams (Agostinho et al., 2004). It is a strategic area for conservation of regional biodiversity and was designated an official environmental protection area in 1997 (APA: ‘‘Area de Protec¸a˜o Ambiental das Ilhas e Va´rzeas do Rio Parana´’’). Its high spatial and temporal environmental heterogeneity sustains a rich biodiversity and the annual flood pulse is the main driver that regulates ecosystem structure and functioning. Despite major regulation of flow by upstream reservoirs, in particular the recently completed Porto Primavera dam, immediately upstream of the active floodplain stretch, summer flood events still occur and vary substantially in amplitude and duration from year to year. When the water level of the Parana´ River surpasses 3.5 m above datum (gauge location at the Nupe´lia field station, Porto Rico: 228450 53.2000 S; 0538150 27.2700 W) connection with its floodplain and marginal habitats increases considerably (Agostinho et al., 2004). When the water level reaches 3.5 m above datum the river-floodplain system is considered to be under the flood influence and intense biotic and abiotic changes are expected to occur. When the water level reaches 4.6 m above datum marginal banks are overflowed and the river-floodplain system becomes intensely connected (Souza-Filho et al., 2004a). In the stretch we studied, monthly mean river flow varies from 7889 m3 s1 (874 SD) to 13,377 m3 s1 (4813 SD) (amplitude: 6713–28,673 m3 s1) (Souza-Filho et al., 2004b). The area of study was centered at 228460 S; 0538190 W, close to the town of Porto Rico in Parana´ State, Brazil (Fig. 1). We selected four habitats known from previous study to be areas dominated by large monospecific stands of Hydrocharitaceae (predominantly E. najas with rare occurrences of Egeria densa, prior to invasion by H.
Fig. 1. Map of the sampling stations: two shallow sites in the Parana´ River (R1 and R2) and two riverine lakes (L1 and L2).
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verticillata). Several species of submersed macrophytes occur in the Parana´-floodplain system, for instance: Heteranthera sp., Bacopa sp., Potamogeton pusillus, Najas microcarpa, Chara guairensis, Nitella furcata, and Cabomba furcata. However they tend to occur in habitats not dominated by monospecific Hydrocharitaceae stands, they are much less frequent and occur with lower biomass. These species do not produce dense canopy-forming stands like the Hydrocharitaceae species do and they apparently cannot compete with E. najas and H. verticillata. So, submersed communities in most sites are dominated mainly by these two species of Hydrocharitaceae. The selected sites represent habitats with two degrees of connections within the river-floodplain system, being located along two shallow banks in the main channel of the Parana´ River (R1 and R2), and in two lakes (L1 and L2) located within a riverine island. The lakes were small (1–2 ha) and permanently connected with the river at their downstream end through a narrow channel (width: 2–5 m). Hence, although the lakes were mainly considered to be lentic waters, their hydrodynamics were strongly influenced by fluctuations in river water level. For instance, intense water exchange between river and lakes occurred owing to the daily water level fluctuations which can reach 1.0 m amplitude in this stretch of the Parana´ River due to flow regulation by upstream hydroelectric reservoirs (Souza-Filho et al., 2004a). 2.2. Data collection From January 2006 to December 2007 we carried out monthly surveys at the four sampling sites. During every survey water physico-chemical variables were measured at sub-surface in each site. Temperature was recorded with an YSI meter (Yellow Springs, OH, USA). The photosynthetically active radiation (PAR; mmol m2 s1) was measured at two depths (0.20 and 0.60 m below water surface) using a LiCor1 (Lincoln, NE, USA) underwater quantum sensor connected to a hand-held meter. The light attenuation coefficient (kd; m1) was calculated using the following equation (Kirk, 1994): lnðI0:2 Þ lnðI0:6 Þ kd ¼ 0:4 where I0.2 and I0.6 are the PARs at depths of 0.20 and 0.60 m, respectively. Due to technical problems, light could not be measured in January, February, March and April 2007. In consequence water transparency was taken as Secchi disk depth and values of kd were generated for these surveys through Secchi disk depth values following the equation (Padial and Thomaz, 2008): kd ¼ 2:00 Secchi0:76
ðn ¼ 2136; r 2 ¼ 0:74; p < 0:01Þ
Water samples were taken for determination of alkalinity using Gran titration (Carmouze, 1994) and for laboratory analysis of total phosphorus (TP) and total nitrogen (TN) following standard methods (Golterman et al., 1978 and Zagatto et al., 1981, respectively). From April 2006 we also collected sediment samples for analysis of proportion of organic matter per unit dry weight of sediment (OMsed; % DW1). This was obtained by gravimetry after burning ca. 0.3 g of sediment in a furnace at 450 8C for 4 h. Field physico-chemistry measurements and samples were always collected between 09:00 and 12:00 on every day of sampling. The water level of the Parana´ River was recorded daily at the Nupe´lia field station gauge, adjacent to the town of Porto Rico (location given above). In each habitat an area of about 1 ha was surveyed by snorkelling in a zigzag fashion and a 0.25 m2 quadrat was used to sample monospecific Hydrocharitaceae stands. The number of samples per habitat per month (mean: 10; SD: 4) varied according
to the size of the habitats and area colonized by the target species. Each habitat was visually divided into three sub-areas (beginning, middle and end) and the number of quadrats sampled in each subarea generally was 3 in the lakes, 4 in R2 and 5 in R1. In each sub-area samples were distributed along depths representative of the area occupied by the Hydrocharitaceae (e.g. shallow, middle and deep parts of the stand). A lead weight attached to a graduated string was placed inside each quadrat and depth and plant maximum heights were measured. Depth was measured by stretching the graduated string vertically up to the water surface. Plant height was measured by stretching string and plant together from plant base to the distal end of the plant (plants were sometimes longer than the total water depth). All above-ground plant material rooted inside each quadrat was harvested. The destructive method to evaluate plant biomass was considered highly unlikely to cause significant damage to the stands since the total area harvested monthly represented a very small proportion (<0.5%) of the total area occupied by the Hydrocharitaceae stands. Attempts were made to not resample the same place successively (this was generally easy to accomplish because the areas previously sampled could be easily recognized from their square-shaped bare substrate, or by the presence of young plants recolonizing previously sampled quadrat locations). Plant samples were washed and species separated back in the laboratory, then dried at c. 80 8C to constant weight for measurement of plant biomass (dry weight: g DW m2). To evaluate macrophyte phenology (e.g. net primary productivity, biomass stagnancy or decay) an estimative of the rate of biomass variation between surveys, here defined as the net biomass increase (NBI; g DW m2 d1), was calculated for each species in each habitat using the equation: W2 W1 NBI ¼ t2 t1 where (W2 W1) is the difference between the mean dry weight of two consecutive surveys and (t2 t1) is the number of days between these surveys. 2.3. Data analyses Two-way analysis of variance (ANOVA) followed by Tukey post hoc testing was applied to assess the effects of habitat types (river and lakes) and hydrological seasons (low-water level and flood periods) on the abiotic variables. Flood periods were defined by the first and last days in a season with water level 3.5 m above datum. T-Testing was used to compare depths where E. najas and H. verticillata were collected. Pearson correlation analysis was employed to search for significant relationships between environmental variables. Multiple linear regression procedures (forward stepwise) were applied to search for sets of explanatory variables which could best predict E. najas and H. verticillata abundance (as biomass) and phenology (as NBI). Besides the environmental variables the biomass of each species was also explored as a predictor for the other species biomass and NBI aiming to search for competitive interactions. To evaluate relationships between hydrological regimes and biotic and environmental variables we utilized the mean water level recorded in the last 30 days prior to the sampling survey. For all analyses we considered significance acceptable at p < 0.05. When required data were log or square root (SqRt) transformed to meet analysis assumptions of data normality and variance homogeneity. The software Statistica 7 for Windows (StatSoft Inc.) was used. 3. Results 3.1. Environmental variables ANOVA detected significant differences between river sites and lakes for light attenuation coefficient (kd), total phosphorus and
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Table 1 Environmental variables (mean standard error) with results from two-way ANOVA (p) and Tukey test for the effect of the habitat type (river sites lakes) and hydrological season (low-water levels and floods). Mean values labelled with the same letter are not significantly different (p > 0.05). Environmental variables
Temperature (8C) kd (m1) TN (mg L1) TP (mg L1) Alkalinity (microeq. L1)* OMsed (% DW1)**
River sites
Lakes
p (ANOVA)
Low-waters
Floods
Low-waters
Floods
Habitat
Season
Interaction
23.9 0.5 a 0.76 0.05 a 0.26 0.01 a 9.7 0.8 a 365 12 1.2 0.3 a
28.7 0.3 b 1.07 0.13 b 0.35 0.01 b 10.6 1.3 ac 357 8 1.8 0.7 a
23.5 0.6 a 1.09 0.06 b 0.28 0.01 ac 16.1 1.4 b 387 14 10.4 0.5 b
28.5 0.2 b 1.33 0.10 b 0.32 0.01 bc 15.0 1.5 bc 336 10 9.5 1.3 b
>0.05 <0.001 >0.05 <0.001 >0.05 <0.001
<0.001 0.001 <0.001 >0.05 >0.05 >0.05
>0.05 >0.05 <0.05 >0.05 >0.05 >0.05
Number of observations (n) per habitat type was 34 during low-water levels and 14 for flood periods (except OMsed, n = 8 for flood periods). *Log and ** square root transformed for analysis.
proportion of organic matter in the sediment while water temperature, alkalinity and total nitrogen did not differ significantly between habitat types (Table 1). In relation to the lakes the river sites had more oligotrophic characteristics. River sites had higher water transparency and lower levels of phosphorus. Sediment organic matter was almost ten times higher in the lakes than in the river (Table 1). Two distinct flood periods occurred during this study (Fig. 2). The first (from December 2005 until April 2006) was a typical flood of the Parana´ River (Agostinho et al., 2004). It was marked by several small flood pulses showing relatively low-water levels (mean: 3.6 0.0 m; max.: 4.8 m above datum). The second flood period, associated with the ENSO event, occurred in a shorter period (January–March 2007) but was much more intense. It comprised a single strong flood pulse with a mean water level of 5.5 0.1 and a peak of 6.0 m above datum. There were significant differences among hydrological seasons for water temperature, kd and TN (Table 1). Water level showed strong significant relationships (p < 0.001) with water temperature (r = 0.50), nitrogen (r = 0.48) and kd (r = 0.40) besides a weak but significant correlation (p < 0.05) with phosphorus (r = 0.20). Temperature was significantly higher during flood periods (summer) and varied in the range of 19–22 8C (June–September surveys) to 26–31 8C (November–April surveys; Fig. 3A). Floods tended to drastically reduce water transparency (as expressed by kd increases) in the whole riverine system (Fig. 3B). After the 2007 flood the water transparency in the lagoons did not improve as fast as it did in the river channel, or as it did after the 2006 flood. The highest concentrations of nitrogen were found during the big flood of 2007 (Fig. 3C) and phosphorus peaked immediately after this flood (Fig. 3D). Alkalinity peaked during the dry period of 2007 (Fig. 3E). Sediment organic matter remained constantly lower in the river sites compared to lake sites (Fig. 3F).
Fig. 2. Parana´ River daily water level (m) measured at the Nupe´lia field station gauge, Porto Rico (228450 53.2000 S; 0538150 27.2700 W).
3.2. Hydrocharitaceae dynamics H. verticillata did not establish in the lakes but dominated the river channel sites (Table 2). E. najas and H. verticillata co-occurred in 30% of the quadrats sampled in the river. In this habitats E. najas occurred in depths (1.9 0.1 m) significantly lower (p < 0.001) than H. verticillata (2.1 0.1 m). However, depths recorded for E. najas in the lakes (2.3 + 0.1 m) did not differ significantly (p > 0.05) from H. verticillata depths in the river. Only eleven samples (out of 368 quadrats sampled in the lakes) of H. verticillata were recorded inside a lake (L2) occurring in depths of 1.6 0.2 m and with very low biomass values (Table 2). E. densa, N. furcata, N. microcarpa, C. guairensis, P. pusillus and C. furcata had rare occurrences (frequency < 2% each) and at very low biomass (<1% of the total). Biomass and height of both species tended to decline in response to flood events and recover with the establishment of low-water levels (Fig. 4A–H). Following flood disturbances species promptly invested in height (vertical growth) while plant biomass had a slower recovery. From January to June 2006 plant biomass and height oscillated in response to the first flood period. Thereafter macrophytes grew to high abundances from November 2006 through January 2007. The major flood pulse of 2007 had a drastic impact on macrophyte populations. In the river plants started to recover from August 2007, but in the lakes no significant growth was noted until the final survey in December 2007. In site R1, before the 2007 flood H. verticillata reached its highest NBI (5.4 g DW m2 d1) from October to November 2006 while its highest biomass (400 102 g DW m2) was obtained in January 2007 (Fig. 4A). In R1 the highest NBI for E. najas (3.7 g DW m2 d1) was recorded from February to March 2006. After the first flood period E. najas developed at a fairly consistent rate, reaching its maximum biomass (171 50 g DW m2) in November 2006 (Fig. 4A). Due to the major flood, from March to September 2007 stands of both species had abundance values close to zero. Both species showed signs of recovery from October 2007. In the river site R1 H. verticillata had its highest NBI (9.5 g DW m2 d1) from October to November 2007 while its biomass peaked in December 2007 with 495 175 g DW m2. In 2007 E. najas reached its peak (151 43 g DW m2) again in November. H. verticillata was not found at R2 in the first two surveys (January–February 2006) and in March and April 2006 the plant appeared in four and three samples, respectively, at relatively low abundance (Fig. 4C). However, from May 2006 H. verticillata started to occur in the majority of the quadrats sampled in R2 and from August 2006 it surpassed E. najas in abundance. Before the major disturbance H. verticillata had reached its highest NBI (6.2 g DW m2 d1) from October to November 2006 and the highest abundance (586 139 g DW m2) in January 2007. In R2, after the 2007 flood H. verticillata showed the first substantial sign of recovery in August 2007. From September to October 2007 H. verticillata had the highest NBI found in the whole study
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Fig. 3. Water physico-chemical variables (mean standard error) for the river sites (R1 and R2) and riverine lakes (L1 and L2): (A) temperature, (B) kd, (C) TN, (D) TP, (E) alkalinity and (F) sediment organic matter. The dotted vertical line represents the first (normal) flood period and the dashed vertical line, the ENSO flood. Months/years are shown on the xaxis.
(19.5 g DW m2 d1), and in November 2007 the highest biomass (1415 255 g DW m2). The greatest development of E. najas in river sites (5.2 g DW m2 d1) occurred in R2 from January to February 2006 (while H. verticillata was still absent) reaching a biomass peak of 333 83 g DW m2 (Fig. 4C). After the 2007 disturbance E. najas showed its first substantial signs of recovery in September 2007 and had its greatest recovery from September to October 2007 (3.3 g DW m2 d1) reaching a biomass of 210 106 g DW m2. Following the first flood period E. najas showed luxuriant growth in both lakes, especially from November through December 2006 (Fig. 4E–H). The maximum development of E. najas recorded during the whole study period occurred at this time in L2 with a NBI of 6.8 g DW m2 d1 and a biomass peak of 628 82 g DW m2. Owing to the 2007 flood not even propagules were found in L1 from May to November 2007 and only one sample of E. najas (<0.1 g DW m2) was recorded in December 2007. In L2 Table 2 Number of quadrats sampled, % of occurrence and biomass (mean standard error; minimum–maximum between brackets) of E. najas and H. verticillata in the river stations and riverine lakes. Habitat
River sites
Lakes
Total of quadrats sampled E. najas occurrence H. verticillata occurrence E. najas biomass (g DW m2) H. verticillata biomass (g DW m2)
573 61% 88% 93 7 (0–775) 235 17 (0–2608)
368 98% 3% 122 11 (0–209) 2 1 (0–7)
plants remained present after the major disturbance but biomass stayed below 1.0 g DW m2 from May through November 2007, reaching 11 5 g DW m2 in December 2007. From October to December 2007 eleven samples of H. verticillata were registered in L2, reaching a peak biomass of only 2.0 1.0 g DW m2 (Fig. 4G). 3.3. Multiple regression analysis Stepwise regression procedures produced best-fit linear models to predict biomass and NBI of both species (Table 3). Three variables, kd, temperature and sediment organic matter, were good predictors in the biomass model of each species, while only one variable was incorporated in the NBI model of each species: water level for E. najas and kd for H. verticillata. While sediment organic matter was the weaker predictor in the model of E. najas biomass (see r2 changes, Table 3) it was the strongest variable in the model of H. verticillata biomass. 4. Discussion The two target species of Hydrocharitaceae showed marked and different patterns of colonization, recovery and abundance in response to temporal and spatial changes in environmental conditions influencing their habitat. E. najas reached the maximum depth of lakes (L1: 3.6 m and L2: 3.0 m) but in the Parana´ River Hydrocharitaceae stands were confined to depths shallower than 4.3 m (outside floods) and the native plant tended to occupy
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Fig. 4. Biomass and heightmax (mean standard error) of H. verticillata and E. najas at the river sites (A–D) and marginal lakes (E–H). The dotted vertical line represents the first (normal) flood period and the dashed vertical line, the ENSO flood. Months/years are shown on the x-axis.
shallower depths than H. verticillata. These colonization depths can be compared with those recorded in the Itaipu Reservoir, at the downstream end of the Upper Parana´ River floodplain, where high turbidity (Secchi depth usually <2.0 m) limited E. najas colonization to depths usually shallower than 3.0–3.5 m (Thomaz and Bini, 1999; Bini and Thomaz, 2005). It does not seem that this depth limit in the Parana´ River is driven by light availability alone because of the high water transparency of this river (usually Secchi depth > 4.0 m). Instead, studies conducted in the Upper Parana´ River (Sousa et al., unpublished data) have shown that maximum colonization depth of submersed macrophytes is probably limited by the scouring forces promoted by water flow, which tend to increase with depth and distance from the river bank. High water flow has been regarded as an important factor limiting macrophyte development in lotic environments elsewhere (e.g. Chambers et al., 1991; Riis and Biggs, 2003; Sand-Jensen, 2008).
Our observations confirm that variations in water level regime lead to major temporal changes in environmental variables and in submersed macrophyte stands. Each flood period affected the vegetation differently. The low intensity flood period (2006) reduced macrophyte abundance in all habitats but not to such an extent that plants were unable to recover quickly afterwards. The 2007 extreme flood, however, almost completely eliminated above-ground plant biomass in all habitats. In the river sites plants took from five to eight months to start to regenerate, while in the lakes no substantial biomass increase was observed after the major flood up to the end of the study period (although by December 2008 Egeria growth was once again luxuriant in the lakes: Murphy and Thomaz, personal observation). When flood pulses occurred the water of the Parana´ River likely received substantial inputs of nutrients and suspended matter as evidenced by rises of phosphorus and nitrogen, as well as a decline in
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Table 3 Models yielded by stepwise regression analysis which explained H. verticillata and E. najas biomass (g DW m2) and net biomass increase rate (NBI; g DW m2 d1). The independent variables analyzed by the regression procedures were water temperature, light attenuation coefficient (kd), alkalinity, total phosphorus and total nitrogen, proportion of organic matter in the sediment (%OMsed), water level of the Parana´ River (mean of the last 30 days prior to the sampling survey) and biomass of H. verticillata and E. najas. Note: b is a measure of the relative contribution of each variable to the model. Dependent variable E. najas (g DW m n = 84
2
)
r2
F
p
Predictor
Coefficient
b
p
r2 change
0.291
10.95
<0.001
Intercept kd Temperature %OMsed
181.6 146.1 15.6 5.6
0.51 0.45 0.24
0.033 <0.001 <0.001 0.016
0.095 0.143 0.053
Intercept %OMsed kd Temperature
83.5 15.2 238.3 21.5
0.31 0.38 0.29
0.628 0.002 <0.001 0.003
0.204 0.074 0.074
H. verticillata (g DW m2) n = 84
0.352
E. najas NBI (g DW m2 d1) n = 92
0.195
2
H. verticillata NBI (g DW m n = 92
d
1
)
0.125
14.47
21.76
12.97
<0.001
<0.001
<0.001
Intercept WL
4.81 1.57
0.44
<0.001 <0.001
0.195
Intercept kd
3.83 3.39
0.35
<0.001 <0.001
0.125
Owing to the lack of %OMsed data for January, February and March 2006 (see Section 2) the regression analyses was firstly run without data from these surveys (n = 84). If %OMsed was not selected as a significant (p < 0.05) predictor then another analyses were run without %OMsed but with data from all surveys (n = 92 for NBI).
transparency. Moreover, elevated water flows and turbulence occasioned intense erosion and deposition processes especially during the major flood. Hence, floods probably impacted both species of Hydrocharitaceae (especially in 2007) through disturbance processes of sediment movement and plant scouring (uprooting), coupled with intense stress caused by low light availability. E. najas and H. verticillata both maximize light acquisition through stem elongation, forming dense and tall canopies, with biomass usually concentrated just below the water surface. Especially during stress periods caused by floods, light acquisition is likely a problem for both species in these riverine habitats, and they respond by growing longer. Following flood disturbances plants invested in shoot elongation prior to significant increases in biomass. Although both species are able to adapt photosynthesis to low light intensities, growth is maximized under higher light availability (Van et al., 1976; Tavechio and Thomaz, 2003). Moreover, the ability to elongate and maintain photosynthetic tissues near the water surface can give a competitive advantage to plants (Haller and Sutton, 1975; Van et al., 1999). Our study recorded biomass values of E. najas and H. verticillata much greater than observed elsewhere (e.g. Bowes et al., 1979; Spencer et al., 1994; Thomaz et al., 1999; Rybicki et al., 2001; Havens, 2003) which highlights the very high productivity of this subtropical riverine floodplain system. Macrophyte biomass peaked during periods of high water temperature and transparency and low-water levels. In the river sites, during the recovery process following flood disturbances the highest increases in biomass of both species occurred when temperature was rising from 24 to 28 8C (October–November 2006) and from 22 to 25 8C (September–October 2007). Although temperature was an important explanatory variable for the biomass of both species it is hard to determine how much this relationship reflects a direct effect of temperature upon plants growth or how much it expresses the effects of altered hydrological regimes on the Hydrocharitaceae stands, since water level regimes have a direct relationship with temperature in the Upper Parana´ system. While the temporal dynamics of the two target species were mainly related to variations in water level, transparency and temperature, sediment organic matter was also a strong predictor of spatial variation for biomass of both species, especially H. verticillata. Propagule availability was not the cause of this plant’s lack of success in colonizing lakes because fragments of Hydrilla were often observed in these habitats, brought in by the daily water exchange with the river channel. Moreover, periodical
surveys showed that up to December 2008 H. verticillata had not yet developed inside lakes (or had only extremely limited presence). Our results suggest that the high sediment organic content was likely hampering Hydrilla growth in the lakes. The negative impact of high sediment organic content upon Hydrilla has been shown experimentally by Barko and Smart (1983, 1986) who cited as one possible explanation the toxicity of compounds generated by anaerobic decomposition. More recently other authors have also demonstrated the effect of anoxia (favoured by organic matter decomposition) on the production of toxic compounds for aquatic plants (e.g. Moore et al., 1992; Pezeshki, 2001; Blokhina et al., 2003). While E. najas dominated the lakes it was likely suffering high competitive pressure from H. verticillata in the Parana´ River channel. The biggest E. najas development in the river sites occurred early in 2006 when H. verticillata was just starting its invasion. The competitive suppression of E. najas by H. verticillata was especially evident in R2 where the highest biomass of E. najas occurred while the invasive species was still absent. After that H. verticillata gradually increased to dominate the area while E. najas stands declined. However, E. najas showed a substantial recovery in both river sites after the major disturbance. These results indicate that major floods might hinder E. najas displacement by H. verticillata. Both species have high dispersal-regeneration ability through stem fragments (Cook and Lu¨o¨nd, 1982; Cook and UrmiKo¨nig, 1984; Rybicki et al., 2001; Thomaz et al., 2006) and since substantial sources of propagules exist plants can easily colonize areas opened up by floods (Combroux et al., 2002). The ability to regenerate after flood disturbance depends on the ecological traits of the species concerned, as well as the intensity of the impact from disturbance (Henry et al., 1996; Bornette et al., 2008). E. najas and H. verticillata demonstrated a substantial capacity for recovery following disturbances and started the regeneration process practically at the same time. After the larger flood event the regeneration process started earliest in the river site R2. The river site R1 was highly impacted by sediment deposition, which probably hampered regeneration. During the major flood, river waters overflowed lake banks intensely scouring vegetation. The scouring process was more intense in lake L1 due to its elongated form parallel to the river flow while lake L2 had a round shape and a narrower river connection channel which was likely to facilitate trapping of propagules. The longer time taken for biomass to recover in the lakes after the ENSO event suggests that these habitats are much less resilient to flood disturbances than are the river channel habitats. Constant propagule inflows via river
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water from reservoirs located upstream (which are densely colonized by submersed plants; Martins et al., 2008) may be important for the faster recovery seen in the river compared to its associated lakes. Regeneration inside the lakes was also probably delayed by a later recovery of water clarity compared with the river sites. For example, from June until December 2007 values of kd were significantly lower (t-test p < 0.001) in the river (mean 0.66 0.07 m1) than in the lakes (mean 1.15 0.06 m1). Some characteristics of H. verticillata compared to E. najas might confer an advantage of the invasive over the native species in regard to its higher growth rates. For example, E. najas carbohydrates are mainly stored in the shoots while H. verticillata can allocate reserves within a developed root system as well as in underground turions (Netherland, 1997; Owens and Madsen, 1998). Carbohydrate storage in below-ground structures is also a plausible explanation for the higher growth achieved by H. verticillata in 2007 compared with 2006. In 2006 H. verticillata apparently invested in its below-ground parts and in ‘‘resistance’’ structures that cannot be uprooted easily, being able to use these reserves to produce photosynthetic structures after the major disturbance and thus helping its fast recovery. Acknowledgements The first author thanks the Brazilian Council of Research (CNPq) and the Coordenadoria de Aperfeic¸oamento de Pessoal de Nı´vel Superior (CAPES) for funding his Ph.D. course. We are also grateful to Msc. Ma´rcio Silveira for helping with field work and laboratory analysis. S.M. Thomaz is a Productivity Researcher from CNPq and acknowledges this agency for constant funding. Survey work was partially funded by CNPq though the Long Term Ecological Research Program (site number 6). References Agostinho, A.A., Gomes, L.C., Verissimo, S., Okada, E.K., 2004. Flood regime, dam regulation and fish in the Upper Parana River: effects on assemblage attributes, reproduction and recruitment. Rev. Fish Biol. Fish. 14, 11–19. Barko, J.W., Smart, R.M., 1981. Comparative influences of light and temperature on the growth and metabolism of selected submersed freshwater macrophytes. Ecol. Monogr. 51, 219–235. Barko, J.W., Smart, R.M., 1983. Effects of organic matter additions to sediment of the growth of aquatic plants. J. Ecol. 71, 161–175. Barko, J.W., Smart, R.M., 1986. Sediment regulates mechanisms of growth limitation in submersed macrophytes. Ecology 67, 1328–1340. Barrat-Segretain, M., Bornette, G., Hering-Vilas-Boˆas, A., 1998. Comparative abilities of vegetative regeneration among aquatic plants growing in disturbed habitats. Aquat. Bot. 60, 201–211. Bini, L.M., Thomaz, S.M., 2005. Prediction of Egeria najas and Egeria densa accurrence in a large subtropical reservoir (Itaipu Reservoir, Brazil-Paraguay). Aquat. Bot. 83, 227–238. Blokhina, O., Virolainen, E., Fagerstedt, K.V., 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. 91, 179–194. Bornette, G., Amoros, C., Castella, C., Beffy, J.L., 1994. Succession and fluctuation in the aquatic vegetation of two former Rhoˆne River channels. Vegetatio 110, 171– 184. Bornette, G., Tabacchi, E., Hupp, C., Puijalon, S., Rostan, C., 2008. A model of plant strategies in fluvial hydrosystems. Freshwater Biol. 53, 1692–1705. Bowes, G., Holaday, S., Haller, W.T., 1979. Seasonal variation in the biomass, tuber density, and photosynthetic metabolism of Hydrilla in three Florida lakes. J. Aquat. Plant Manage. 15, 32–35. Chambers, P.A., Prepas, E.E., Hamilton, H.R., Bothwell, M.L., 1991. Current velocity and its effect on aquatic macrophytes in flowing waters. Ecol. Appl. 1, 249–257. Carmouze, J.P., 1994. O metabolismo dos ecossistemas aqua´ticos. Edgard Blu¨cher/ SBL/FABESP, Sa˜o Paulo. Combroux, I.C.S., Bornette, G., Amoros, C., 2002. Plant regenerative strategies after a major disturbance: the case of a riverine wetland restoration. Wetlands 22, 234–246. Connell, J.H., 1978. Diversity in tropical rain forest and coral reefs. Science 199, 1302–1310. Cook, C.D.K., Lu¨o¨nd, R., 1982. A revision of the genus Hydrilla (Hydrocharitaceae). Aquat. Bot. 13, 485–504. Cook, C.D.K., Urmi-Ko¨nig, K., 1984. A revision of the genus Egeria (Hydrocharitaceae). Aquat. Bot. 19, 73–96.
47
Golterman, H.L., Clymo, R.S., Ohmstad, M.M., 1978. Methods for Physical and Chemical Analysis of Fresh Waters. Blackwell Scientific Publications, Oxford. Haller, W.T., Sutton, D.L., 1975. Community structure and competition between Hydrilla and Vallisneria. J. Aquat. Plant Manage. 13, 48–50. Havens, K.E., 2003. Submersed aquatic vegetation correlation with depth and light attenuating materials in a shallow subtropical lake. Hydrobiologia 493, 173– 186. Henry, C.P., Amoros, C., Bornette, G., 1996. Species traits and recolonization process after flood disturbances in riverine macrophytes. Vegetatio 122, 13–27. Hershner, C., Havens, K.J., 2008. Managing invasive aquatic plants in a changing system: strategic consideration of ecosystem services. Conserv. Biol. 22, 544– 550. Junk, W.J., Bayley, P.B., Sparks, R.E., 1989. The flood pulse concept in river-floodplain systems. Can. Spec. Publ. Fish. Aquat. Sci. 106, 110–127. Kahara, S.N., Vermaat, J.E., 2003. The effect of alkalinity on photosynthesis-light curves and inorganic carbon extraction capacity of freshwater macrophytes. Aquat. Bot. 75, 217–227. Kirk, J.T.O., 1994. Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Cambridge. Madsen, J.D., Smith, D.H., 1999. Vegetative spread of dioecious Hydrilla colonies in experimental pounds. J. Aquat. Plant Manage. 37, 25–29. Maltchik, L., Rolon, A.S., Schott, P., 2007. Effects of hydrological variation on the aquatic plant community in a floodplain palustrine wetland of southern Brazil. Limnology 8, 23–28. Martins, D., Marchi, S.R., Costa, N.V., 2005. Estudo da movimentac¸a˜o de plantas aqua´ticas imersas presentes no reservato´rio da UHE Eng. Souza Dias – Jupia´ Planta Daninha 23, 351–358. Martins, D., Costa, N.V., Terra, M.A., Marchi, S.R., 2008. Characterization of the aquatic plant communities of 18 reservoirs of five watersheds in Sa˜ol Paulo, Brazil. Planta Daninha 26, 17–32. Mony, C., Koschnick, T.J., Haller, W.T., Muller, S., 2007. Competition between two invasive (Hydrocharitaceae Hydrilla verticillata (L.f.) (Royle) and Egeria densa (Planch)) as influenced by sediment fertility and season. Aquat. Bot. 86, 236– 242. Moore, P.A., Reddy, K.R., Graetz, D.A., 1992. Water quality—nutrient transformations in sediments as influenced by oxygen supply. J. Environ. Qual. 21, 387– 393. Mullin, B.H., Anderson, L.W.J., DiTomaso, J.M., Eplee, R.E., Getsinger, K.D., 2000. Invasive plant species. CAST 13, 1–18. Murphy, K.J., 1988. Aquatic weed problems and their management: a review. I. The worldwide scale of the aquatic weed problem. Crop Prot. 7, 232–248. Murphy, K.J., Pieterse, A.H., 1990. Present status and prospects of integrated control of aquatic weeds. In: Pieterse, A.H., Murphy, K.J. (Eds.), The Ecology and Management of Nuisance Aquatic Vegetation. Oxford Publications, New York, pp. 222–227. Neiff, J.J., 1990. Ideas para la interpretacion ecologica del Parana´. Interciencia 15, 424–441. Netherland, M.D., 1997. Turion ecology of Hydrilla. J. Aquat. Plant Manage. 35, 1–10. Owens, C.S., Madsen, J.D., 1998. Phenological studies of carbohydrate allocation in Hydrilla. J. Aquat. Plant Manage. 36, 40–44. Padial, A.A., Thomaz, S.M., 2008. Prediction of the light attenuation coefficient through the Secchi disk depth: empirical modeling in two large Neotropical ecosystems. Limnology 9, 143–151. Pezeshki, S.R., 2001. Wetland plant responses to soil flooding. Environ. Exp. Bot. 46, 299–312. Pierini, S.A., Thomaz, S.M., 2004. Effects of inorganic carbon source on photosynthetic rates of Egeria najas Planchon and Egeria densa Planchon (Hydrocharitaceae). Aquat. Bot. 78, 135–146. Riis, T., Biggs, B.J.F., 2003. Hydrologic and hydraulic control of macrophyte establishment and performance in streams. Limnol. Oceanogr. 48, 1488– 1497. Rybicki, N.B., McFarland, D.G., Ruhl, H.A., Reel, J.T., Barko, J.W., 2001. Investigations of the availability and survival of submersed aquatic vegetation propagules in the tidal Potamic River. Estuaries 24, 407–427. Sand-Jensen, K., 2008. Drag forces on common plant species in temperate streams: consequences of morphology, velocity and biomass. Hydrobiologia 610, 307– 319. Santos, A.M., Thomaz, S.M., 2007. Aquatic macrophytes diversity in lagoons of a tropical floodplain: the role of connectivity and water level. Aust. Ecol. 32, 177– 190. Souza-Filho, E.E., Comunello, E., Rocha, P.C., 2004a. Flood extension in the BaiaCurutuba-Ivinheima complex of the Parana River Floodplain. In: Agostinho, A.A., Rodrigues, L., Gomes, L.C., Thomaz, S.M., Miranda, L.A. (Eds.), Structure and Functioning of the Parana´ River and its Floodplain: LTER – Site 6 – (PELD – Sı´tio 6). Eduem, Maringa´, pp. 19–24. Souza-Filho, E.E., Rocha, P.C., Comunello, E., Stevaux, J.C., 2004b. Effects of the Porto Primavera Dam on physical environment of the downstream floodplain. In: Thomaz, S.M., Agostinho, A.A., Hahn, N.S. (Eds.), The Upper Parana´ River and its Floodplain: Physical Aspects, Ecology and Conservation. Blackhuys, Liden, pp. 55–74. Spencer, W.E., Teeri, J., Wetzel, R.G., 1994. Acclimation of photosynthetic phenotype to environmental heterogeneity. Ecology 75, 301–314. Tavechio, W.L.G., Thomaz, S.M., 2003. Effects of light on the growth of Egeria najas Planchon. Braz. Arch. Biol. Technol. 46, 203–209. Thomaz, S.M., Bini, L.M., 1999. A expansa˜o das macro´fitas aqua´ticas e implicac¸o˜es para o manejo de reservato´rios: um estudo na represa de Itaipu. In: Henry, R.
48
W.T.Z. Sousa et al. / Aquatic Botany 92 (2010) 40–48
(Ed.), Ecologia de Reservato´rios: Estrutura, Func¸a˜o e Aspectos Sociais. FAPESP/ Fundibio, Botucatu, pp. 599–625. Thomaz, S.M., Bini, L.M., Souza, M.C., Kita, K.K., Camargo, A.F.M., 1999. Aquatic macrophytes of Itaipu reservoir, Brazil: surveys of species and ecological considerations. Braz. Arch. Biol. Technol. 42, 15–22. Thomaz, S.M., Pagioro, T.A., Bini, L.M., Murphy, K.J., 2006. Effect of reservoir drawdown on biomass of three species of aquatic macrophytes in a large sub-tropical reservoir (Itaipu, Brazil). Hydrobiologia 570, 53–59. Thomaz, S.M., Bini, L.M., Bozelli, R.L., 2007. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia 579, 1–13. Thomaz, S.M., Carvalho, P., Padial, A.A., Kobayashi, J.T., 2009. Macrophytes in the Upper Parana´ River floodplain: long term patterns over large spatial scales. Braz. J. Biol. 69, 617–625. Van, T.K., Haller, W.T., Bowes, G., 1976. Comparison of the photosynthetic characteristics of three submersed aquatic plants. Plant Physiol. 58, 761–768.
Van, T.K., Wheeler, G.S., Center, T.D., 1999. Competition between Hydrilla verticillata and Vallisneria americana as influenced by soil fertility. Aquat. Bot. 62, 225–233. Van Geest, G.J., Wolters, H., Roozen, F.C.J.M., Coops, H., Roijackers, R.M.M., Buijse, A.D., Scheffer, M., 2005. Water-level fluctuations affect macrophyte richness in floodplain lakes. Hydrobiologia 539, 239–248. Wang, J., Yu, D., Xiong, W., Han, Y., 2008. Above- and belowground competition between two submersed macrophytes. Hydrobiologia 607, 113–122. Ward, J.V., Tockner, K., Arscott, D.B., Claret, C., 2002. Riverine landscape diversity. Freshwater Biol. 47, 517–539. Wingfield, R., Murphy, K.J., Gaywood, M., 2006. Assessing and predicting the success of Najas flexilis (Willd.) Rostk. & Schimidt, a rare European aquatic macrophyte, in relation to lake environmental conditions. Hydrobiologia 570, 79–86. Zagatto, E.A.G., Jacintho, A.O., Reis, B.F., Krug, F.J., Bergamin, H., Pessenda, L.C., Mortatti, R.J., Gine´, M.F., 1981. Manual de ana´lises de plantas empregando sistemas de injec¸a˜o em fluxo. USP, Piracicaba.
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Aquatic Botany journal homepage: www.elsevier.com/locate/aquabot
Response of native Egeria najas Planch. and invasive Hydrilla verticillata (L.f.) Royle to altered hydroecological regime in a subtropical river Wilson Treger Z. Sousa a,*, Sidinei M. Thomaz a, Kevin J. Murphy b a b
Universidade Estadual de Maringa´, Nupe´lia, Av. Colombo 5790, 87020-900 Maringa´, Pr, Brazil Division of Ecology and Evolutionary Biology, Faculty of Biomedical and Life Sciences, University of Glasgow G12 8QQ, Scotland, UK
A R T I C L E I N F O
A B S T R A C T
Article history: Received 4 March 2009 Received in revised form 29 September 2009 Accepted 5 October 2009 Available online 12 October 2009
Egeria najas Planch. is the dominant native submersed macrophyte of the Upper Parana´ River in Brazil, while Hydrilla verticillata (L.f.) Royle has recently invaded this area. From January 2006 to December 2007, comprising two annual flood cycles, we conducted monthly surveys at two river stations and two lakes connected to the river within this stretch of the Parana´ River, aiming to understand how the hydrological regime influences the distribution and abundance of these native and invasive Hydrocharitaceae species. Hydrilla did not develop in the lakes, possibly due to the elevated proportion of organic matter in the sediment (10% DW). However, the exotic species dominated the river sites apparently suppressing E. najas. In the lakes E. najas reached a maximum biomass of 628 82 g DW m2 but did not surpass 333 83 g DW m2 in the river, where H. verticillata peaked at 1415 255 g DW m2. Macrophyte biomass development was greatest during low-water periods, with transparent water and high temperatures. Floods probably affected submersed macrophytes (especially in 2007, when an extreme flood caused by an El Nin˜o Southern Oscillation (ENSO) event occurred) via sediment movement and plant scouring (uprooting) effects, coupled with reduced water transparency. Macrophyte recovery started soon after the (less intense) 2006 flood but was delayed in 2007. In the river recovery started five months after the major flood, but in the lakes no significant plant regeneration was found even nine months after the disturbance. E. najas and H. verticillata started regeneration practically at the same time but H. verticillata had much higher rates of biomass increase. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Hydrocharitaceae Biomass Flood disturbance Regeneration Riverine floodplain ENSO
1. Introduction Hydrilla verticillata (L.f.) Royle, one of the most successful aquatic weeds in the world (Murphy, 1988; Mullin et al., 2000; Hershner and Havens, 2008), is newly invasive in the Upper Parana´ River catchment (first recorded in June 2005: Thomaz et al., 2009). Egeria najas Planch. is the dominant native submersed plant in this river and its associated floodplain waterbodies. Although it is regarded as a potential nuisance species that can cause localized problems in reservoirs (Thomaz and Bini, 1999; Martins et al., 2005, 2008), E. najas is not invasive outside its native range of southern Brazil, north east Argentina and Paraguay (Cook and Urmi-Ko¨nig, 1984). Both species are members of the family Hydrocharitaceae with very similar morphology and ecological characteristics. They grow vertically in the water column, forming
* Corresponding author. Tel.: +55 44 3261 4616. E-mail addresses: [email protected] (W.T.Z. Sousa), [email protected] (S.M. Thomaz), [email protected] (K.J. Murphy). 0304-3770/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.aquabot.2009.10.002
dense canopies near the water surface and show physiological plasticity which enables growth under low levels of light and inorganic carbon (Van et al., 1976; Barko and Smart, 1981; Spencer et al., 1994; Kahara and Vermaat, 2003; Tavechio and Thomaz, 2003; Pierini and Thomaz, 2004). However, unlike E. najas, H. verticillata has specialized structures for vegetative reproduction (tubers and turions) besides a well-developed rhizome system capable of stocking carbohydrate reserves which enable the plant to persist and recover quickly even after severe disturbances (Owens and Madsen, 1998; Madsen and Smith, 1999). H. verticillata can potentially displace native submersed macrophyte communities (Van et al., 1999; Mony et al., 2007; Wang et al., 2008). Since E. najas and H. verticillata display very similar ecological strategies and growth form, competitive interaction could be intense. While H. verticillata is one of the most extensively studied aquatic macrophytes, there is only scarce information about the biology and ecology of E. najas (e.g. Tavechio and Thomaz, 2003; Pierini and Thomaz, 2004), especially in its native habitats (Bini and Thomaz, 2005; Thomaz et al., 2006). Improved understanding of which factors affect the population
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dynamics of these native and exotic Hydrocharitaceae can help in the development of conservation and management plans (Murphy and Pieterse, 1990; Wingfield et al., 2006). Hydrological regime is considered the key factor driving ecological functioning and biodiversity patterns in river-floodplain systems (Junk et al., 1989; Neiff, 1990; Ward et al., 2002; Thomaz et al., 2007). Variations in water level potentially lead to significant changes in aquatic plant communities (Bornette et al., 1994; Van Geest et al., 2005; Maltchik et al., 2007; Santos and Thomaz, 2007). According to the intermediate disturbance hypothesis (Connell, 1978), hydrological disturbances tend to disrupt competitive processes among aquatic plants opening gaps for colonization and development of less competitive species (Junk et al., 1989; Bornette et al., 1994; Santos and Thomaz, 2007). For example, after flood disturbances in a former channel of the Rhoˆne River, France, Henry et al. (1996) found that the first species to reestablish were able to produce turions or other non-subterranean vegetative organs. Hence, in the Upper Parana´ River floodplain, flood disturbances could help to prevent competitive exclusion of native species by H. verticillata or conversely might accelerate exclusion processes, if the recovery rate of the exotic plant is much quicker than that of the native plants (Henry et al., 1996; BarratSegretain et al., 1998; Bornette et al., 2008). In this investigation we monitored the environmental parameters and the dynamics (biomass and height) of monospecific Hydrocharitaceae stands over 24 months in two sites of the Parana´ River and two connected lakes aiming to understand how the hydrological regime influences the distribution and abundance of E. najas and H. verticillata. The river sites and connected lakes represent two types of floodplain habitats characterized by different degrees of connectivity with the river and thus presenting different environmental characteristics such as hydrology (e.g. lotic vs. semi-lentic) and geomorphology (e.g. open vs. protected areas). The specific questions of this study are (1) is there a difference between the native and the invasive Hydrocharitaceae regarding their spatial and temporal patterns of distribution and abundance (e.g. response to flood disturbances)?; (2) is there a difference between river sites and connected lakes concerning the macrophyte dynamics (e.g. resilience to flood disturbances)?; (3) which environmental variables can best explain E. najas and H. verticillata biomass and rate of net biomass increase (NBI)? and (4) what are the effects of intra-annual (seasonal water level
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˜ o South Oscillation variations) and inter-annual (normal vs. El Nin (ENSO) flood) on macrophytes in two categories of sites (lakes vs. river)? Our results are also of interest because during the study period we had the opportunity to assess the effects of an extreme, low recurrence flood, caused by an ENSO, which happens every 5–7 years in the Parana´ River system. 2. Materials and methods 2.1. Study area The Upper Parana´ River floodplain is the only remaining stretch (about 230 km long and up to 20 km wide) of the river inside Brazil without dams (Agostinho et al., 2004). It is a strategic area for conservation of regional biodiversity and was designated an official environmental protection area in 1997 (APA: ‘‘Area de Protec¸a˜o Ambiental das Ilhas e Va´rzeas do Rio Parana´’’). Its high spatial and temporal environmental heterogeneity sustains a rich biodiversity and the annual flood pulse is the main driver that regulates ecosystem structure and functioning. Despite major regulation of flow by upstream reservoirs, in particular the recently completed Porto Primavera dam, immediately upstream of the active floodplain stretch, summer flood events still occur and vary substantially in amplitude and duration from year to year. When the water level of the Parana´ River surpasses 3.5 m above datum (gauge location at the Nupe´lia field station, Porto Rico: 228450 53.2000 S; 0538150 27.2700 W) connection with its floodplain and marginal habitats increases considerably (Agostinho et al., 2004). When the water level reaches 3.5 m above datum the river-floodplain system is considered to be under the flood influence and intense biotic and abiotic changes are expected to occur. When the water level reaches 4.6 m above datum marginal banks are overflowed and the river-floodplain system becomes intensely connected (Souza-Filho et al., 2004a). In the stretch we studied, monthly mean river flow varies from 7889 m3 s1 (874 SD) to 13,377 m3 s1 (4813 SD) (amplitude: 6713–28,673 m3 s1) (Souza-Filho et al., 2004b). The area of study was centered at 228460 S; 0538190 W, close to the town of Porto Rico in Parana´ State, Brazil (Fig. 1). We selected four habitats known from previous study to be areas dominated by large monospecific stands of Hydrocharitaceae (predominantly E. najas with rare occurrences of Egeria densa, prior to invasion by H.
Fig. 1. Map of the sampling stations: two shallow sites in the Parana´ River (R1 and R2) and two riverine lakes (L1 and L2).
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verticillata). Several species of submersed macrophytes occur in the Parana´-floodplain system, for instance: Heteranthera sp., Bacopa sp., Potamogeton pusillus, Najas microcarpa, Chara guairensis, Nitella furcata, and Cabomba furcata. However they tend to occur in habitats not dominated by monospecific Hydrocharitaceae stands, they are much less frequent and occur with lower biomass. These species do not produce dense canopy-forming stands like the Hydrocharitaceae species do and they apparently cannot compete with E. najas and H. verticillata. So, submersed communities in most sites are dominated mainly by these two species of Hydrocharitaceae. The selected sites represent habitats with two degrees of connections within the river-floodplain system, being located along two shallow banks in the main channel of the Parana´ River (R1 and R2), and in two lakes (L1 and L2) located within a riverine island. The lakes were small (1–2 ha) and permanently connected with the river at their downstream end through a narrow channel (width: 2–5 m). Hence, although the lakes were mainly considered to be lentic waters, their hydrodynamics were strongly influenced by fluctuations in river water level. For instance, intense water exchange between river and lakes occurred owing to the daily water level fluctuations which can reach 1.0 m amplitude in this stretch of the Parana´ River due to flow regulation by upstream hydroelectric reservoirs (Souza-Filho et al., 2004a). 2.2. Data collection From January 2006 to December 2007 we carried out monthly surveys at the four sampling sites. During every survey water physico-chemical variables were measured at sub-surface in each site. Temperature was recorded with an YSI meter (Yellow Springs, OH, USA). The photosynthetically active radiation (PAR; mmol m2 s1) was measured at two depths (0.20 and 0.60 m below water surface) using a LiCor1 (Lincoln, NE, USA) underwater quantum sensor connected to a hand-held meter. The light attenuation coefficient (kd; m1) was calculated using the following equation (Kirk, 1994): lnðI0:2 Þ lnðI0:6 Þ kd ¼ 0:4 where I0.2 and I0.6 are the PARs at depths of 0.20 and 0.60 m, respectively. Due to technical problems, light could not be measured in January, February, March and April 2007. In consequence water transparency was taken as Secchi disk depth and values of kd were generated for these surveys through Secchi disk depth values following the equation (Padial and Thomaz, 2008): kd ¼ 2:00 Secchi0:76
ðn ¼ 2136; r 2 ¼ 0:74; p < 0:01Þ
Water samples were taken for determination of alkalinity using Gran titration (Carmouze, 1994) and for laboratory analysis of total phosphorus (TP) and total nitrogen (TN) following standard methods (Golterman et al., 1978 and Zagatto et al., 1981, respectively). From April 2006 we also collected sediment samples for analysis of proportion of organic matter per unit dry weight of sediment (OMsed; % DW1). This was obtained by gravimetry after burning ca. 0.3 g of sediment in a furnace at 450 8C for 4 h. Field physico-chemistry measurements and samples were always collected between 09:00 and 12:00 on every day of sampling. The water level of the Parana´ River was recorded daily at the Nupe´lia field station gauge, adjacent to the town of Porto Rico (location given above). In each habitat an area of about 1 ha was surveyed by snorkelling in a zigzag fashion and a 0.25 m2 quadrat was used to sample monospecific Hydrocharitaceae stands. The number of samples per habitat per month (mean: 10; SD: 4) varied according
to the size of the habitats and area colonized by the target species. Each habitat was visually divided into three sub-areas (beginning, middle and end) and the number of quadrats sampled in each subarea generally was 3 in the lakes, 4 in R2 and 5 in R1. In each sub-area samples were distributed along depths representative of the area occupied by the Hydrocharitaceae (e.g. shallow, middle and deep parts of the stand). A lead weight attached to a graduated string was placed inside each quadrat and depth and plant maximum heights were measured. Depth was measured by stretching the graduated string vertically up to the water surface. Plant height was measured by stretching string and plant together from plant base to the distal end of the plant (plants were sometimes longer than the total water depth). All above-ground plant material rooted inside each quadrat was harvested. The destructive method to evaluate plant biomass was considered highly unlikely to cause significant damage to the stands since the total area harvested monthly represented a very small proportion (<0.5%) of the total area occupied by the Hydrocharitaceae stands. Attempts were made to not resample the same place successively (this was generally easy to accomplish because the areas previously sampled could be easily recognized from their square-shaped bare substrate, or by the presence of young plants recolonizing previously sampled quadrat locations). Plant samples were washed and species separated back in the laboratory, then dried at c. 80 8C to constant weight for measurement of plant biomass (dry weight: g DW m2). To evaluate macrophyte phenology (e.g. net primary productivity, biomass stagnancy or decay) an estimative of the rate of biomass variation between surveys, here defined as the net biomass increase (NBI; g DW m2 d1), was calculated for each species in each habitat using the equation: W2 W1 NBI ¼ t2 t1 where (W2 W1) is the difference between the mean dry weight of two consecutive surveys and (t2 t1) is the number of days between these surveys. 2.3. Data analyses Two-way analysis of variance (ANOVA) followed by Tukey post hoc testing was applied to assess the effects of habitat types (river and lakes) and hydrological seasons (low-water level and flood periods) on the abiotic variables. Flood periods were defined by the first and last days in a season with water level 3.5 m above datum. T-Testing was used to compare depths where E. najas and H. verticillata were collected. Pearson correlation analysis was employed to search for significant relationships between environmental variables. Multiple linear regression procedures (forward stepwise) were applied to search for sets of explanatory variables which could best predict E. najas and H. verticillata abundance (as biomass) and phenology (as NBI). Besides the environmental variables the biomass of each species was also explored as a predictor for the other species biomass and NBI aiming to search for competitive interactions. To evaluate relationships between hydrological regimes and biotic and environmental variables we utilized the mean water level recorded in the last 30 days prior to the sampling survey. For all analyses we considered significance acceptable at p < 0.05. When required data were log or square root (SqRt) transformed to meet analysis assumptions of data normality and variance homogeneity. The software Statistica 7 for Windows (StatSoft Inc.) was used. 3. Results 3.1. Environmental variables ANOVA detected significant differences between river sites and lakes for light attenuation coefficient (kd), total phosphorus and
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Table 1 Environmental variables (mean standard error) with results from two-way ANOVA (p) and Tukey test for the effect of the habitat type (river sites lakes) and hydrological season (low-water levels and floods). Mean values labelled with the same letter are not significantly different (p > 0.05). Environmental variables
Temperature (8C) kd (m1) TN (mg L1) TP (mg L1) Alkalinity (microeq. L1)* OMsed (% DW1)**
River sites
Lakes
p (ANOVA)
Low-waters
Floods
Low-waters
Floods
Habitat
Season
Interaction
23.9 0.5 a 0.76 0.05 a 0.26 0.01 a 9.7 0.8 a 365 12 1.2 0.3 a
28.7 0.3 b 1.07 0.13 b 0.35 0.01 b 10.6 1.3 ac 357 8 1.8 0.7 a
23.5 0.6 a 1.09 0.06 b 0.28 0.01 ac 16.1 1.4 b 387 14 10.4 0.5 b
28.5 0.2 b 1.33 0.10 b 0.32 0.01 bc 15.0 1.5 bc 336 10 9.5 1.3 b
>0.05 <0.001 >0.05 <0.001 >0.05 <0.001
<0.001 0.001 <0.001 >0.05 >0.05 >0.05
>0.05 >0.05 <0.05 >0.05 >0.05 >0.05
Number of observations (n) per habitat type was 34 during low-water levels and 14 for flood periods (except OMsed, n = 8 for flood periods). *Log and ** square root transformed for analysis.
proportion of organic matter in the sediment while water temperature, alkalinity and total nitrogen did not differ significantly between habitat types (Table 1). In relation to the lakes the river sites had more oligotrophic characteristics. River sites had higher water transparency and lower levels of phosphorus. Sediment organic matter was almost ten times higher in the lakes than in the river (Table 1). Two distinct flood periods occurred during this study (Fig. 2). The first (from December 2005 until April 2006) was a typical flood of the Parana´ River (Agostinho et al., 2004). It was marked by several small flood pulses showing relatively low-water levels (mean: 3.6 0.0 m; max.: 4.8 m above datum). The second flood period, associated with the ENSO event, occurred in a shorter period (January–March 2007) but was much more intense. It comprised a single strong flood pulse with a mean water level of 5.5 0.1 and a peak of 6.0 m above datum. There were significant differences among hydrological seasons for water temperature, kd and TN (Table 1). Water level showed strong significant relationships (p < 0.001) with water temperature (r = 0.50), nitrogen (r = 0.48) and kd (r = 0.40) besides a weak but significant correlation (p < 0.05) with phosphorus (r = 0.20). Temperature was significantly higher during flood periods (summer) and varied in the range of 19–22 8C (June–September surveys) to 26–31 8C (November–April surveys; Fig. 3A). Floods tended to drastically reduce water transparency (as expressed by kd increases) in the whole riverine system (Fig. 3B). After the 2007 flood the water transparency in the lagoons did not improve as fast as it did in the river channel, or as it did after the 2006 flood. The highest concentrations of nitrogen were found during the big flood of 2007 (Fig. 3C) and phosphorus peaked immediately after this flood (Fig. 3D). Alkalinity peaked during the dry period of 2007 (Fig. 3E). Sediment organic matter remained constantly lower in the river sites compared to lake sites (Fig. 3F).
Fig. 2. Parana´ River daily water level (m) measured at the Nupe´lia field station gauge, Porto Rico (228450 53.2000 S; 0538150 27.2700 W).
3.2. Hydrocharitaceae dynamics H. verticillata did not establish in the lakes but dominated the river channel sites (Table 2). E. najas and H. verticillata co-occurred in 30% of the quadrats sampled in the river. In this habitats E. najas occurred in depths (1.9 0.1 m) significantly lower (p < 0.001) than H. verticillata (2.1 0.1 m). However, depths recorded for E. najas in the lakes (2.3 + 0.1 m) did not differ significantly (p > 0.05) from H. verticillata depths in the river. Only eleven samples (out of 368 quadrats sampled in the lakes) of H. verticillata were recorded inside a lake (L2) occurring in depths of 1.6 0.2 m and with very low biomass values (Table 2). E. densa, N. furcata, N. microcarpa, C. guairensis, P. pusillus and C. furcata had rare occurrences (frequency < 2% each) and at very low biomass (<1% of the total). Biomass and height of both species tended to decline in response to flood events and recover with the establishment of low-water levels (Fig. 4A–H). Following flood disturbances species promptly invested in height (vertical growth) while plant biomass had a slower recovery. From January to June 2006 plant biomass and height oscillated in response to the first flood period. Thereafter macrophytes grew to high abundances from November 2006 through January 2007. The major flood pulse of 2007 had a drastic impact on macrophyte populations. In the river plants started to recover from August 2007, but in the lakes no significant growth was noted until the final survey in December 2007. In site R1, before the 2007 flood H. verticillata reached its highest NBI (5.4 g DW m2 d1) from October to November 2006 while its highest biomass (400 102 g DW m2) was obtained in January 2007 (Fig. 4A). In R1 the highest NBI for E. najas (3.7 g DW m2 d1) was recorded from February to March 2006. After the first flood period E. najas developed at a fairly consistent rate, reaching its maximum biomass (171 50 g DW m2) in November 2006 (Fig. 4A). Due to the major flood, from March to September 2007 stands of both species had abundance values close to zero. Both species showed signs of recovery from October 2007. In the river site R1 H. verticillata had its highest NBI (9.5 g DW m2 d1) from October to November 2007 while its biomass peaked in December 2007 with 495 175 g DW m2. In 2007 E. najas reached its peak (151 43 g DW m2) again in November. H. verticillata was not found at R2 in the first two surveys (January–February 2006) and in March and April 2006 the plant appeared in four and three samples, respectively, at relatively low abundance (Fig. 4C). However, from May 2006 H. verticillata started to occur in the majority of the quadrats sampled in R2 and from August 2006 it surpassed E. najas in abundance. Before the major disturbance H. verticillata had reached its highest NBI (6.2 g DW m2 d1) from October to November 2006 and the highest abundance (586 139 g DW m2) in January 2007. In R2, after the 2007 flood H. verticillata showed the first substantial sign of recovery in August 2007. From September to October 2007 H. verticillata had the highest NBI found in the whole study
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Fig. 3. Water physico-chemical variables (mean standard error) for the river sites (R1 and R2) and riverine lakes (L1 and L2): (A) temperature, (B) kd, (C) TN, (D) TP, (E) alkalinity and (F) sediment organic matter. The dotted vertical line represents the first (normal) flood period and the dashed vertical line, the ENSO flood. Months/years are shown on the xaxis.
(19.5 g DW m2 d1), and in November 2007 the highest biomass (1415 255 g DW m2). The greatest development of E. najas in river sites (5.2 g DW m2 d1) occurred in R2 from January to February 2006 (while H. verticillata was still absent) reaching a biomass peak of 333 83 g DW m2 (Fig. 4C). After the 2007 disturbance E. najas showed its first substantial signs of recovery in September 2007 and had its greatest recovery from September to October 2007 (3.3 g DW m2 d1) reaching a biomass of 210 106 g DW m2. Following the first flood period E. najas showed luxuriant growth in both lakes, especially from November through December 2006 (Fig. 4E–H). The maximum development of E. najas recorded during the whole study period occurred at this time in L2 with a NBI of 6.8 g DW m2 d1 and a biomass peak of 628 82 g DW m2. Owing to the 2007 flood not even propagules were found in L1 from May to November 2007 and only one sample of E. najas (<0.1 g DW m2) was recorded in December 2007. In L2 Table 2 Number of quadrats sampled, % of occurrence and biomass (mean standard error; minimum–maximum between brackets) of E. najas and H. verticillata in the river stations and riverine lakes. Habitat
River sites
Lakes
Total of quadrats sampled E. najas occurrence H. verticillata occurrence E. najas biomass (g DW m2) H. verticillata biomass (g DW m2)
573 61% 88% 93 7 (0–775) 235 17 (0–2608)
368 98% 3% 122 11 (0–209) 2 1 (0–7)
plants remained present after the major disturbance but biomass stayed below 1.0 g DW m2 from May through November 2007, reaching 11 5 g DW m2 in December 2007. From October to December 2007 eleven samples of H. verticillata were registered in L2, reaching a peak biomass of only 2.0 1.0 g DW m2 (Fig. 4G). 3.3. Multiple regression analysis Stepwise regression procedures produced best-fit linear models to predict biomass and NBI of both species (Table 3). Three variables, kd, temperature and sediment organic matter, were good predictors in the biomass model of each species, while only one variable was incorporated in the NBI model of each species: water level for E. najas and kd for H. verticillata. While sediment organic matter was the weaker predictor in the model of E. najas biomass (see r2 changes, Table 3) it was the strongest variable in the model of H. verticillata biomass. 4. Discussion The two target species of Hydrocharitaceae showed marked and different patterns of colonization, recovery and abundance in response to temporal and spatial changes in environmental conditions influencing their habitat. E. najas reached the maximum depth of lakes (L1: 3.6 m and L2: 3.0 m) but in the Parana´ River Hydrocharitaceae stands were confined to depths shallower than 4.3 m (outside floods) and the native plant tended to occupy
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Fig. 4. Biomass and heightmax (mean standard error) of H. verticillata and E. najas at the river sites (A–D) and marginal lakes (E–H). The dotted vertical line represents the first (normal) flood period and the dashed vertical line, the ENSO flood. Months/years are shown on the x-axis.
shallower depths than H. verticillata. These colonization depths can be compared with those recorded in the Itaipu Reservoir, at the downstream end of the Upper Parana´ River floodplain, where high turbidity (Secchi depth usually <2.0 m) limited E. najas colonization to depths usually shallower than 3.0–3.5 m (Thomaz and Bini, 1999; Bini and Thomaz, 2005). It does not seem that this depth limit in the Parana´ River is driven by light availability alone because of the high water transparency of this river (usually Secchi depth > 4.0 m). Instead, studies conducted in the Upper Parana´ River (Sousa et al., unpublished data) have shown that maximum colonization depth of submersed macrophytes is probably limited by the scouring forces promoted by water flow, which tend to increase with depth and distance from the river bank. High water flow has been regarded as an important factor limiting macrophyte development in lotic environments elsewhere (e.g. Chambers et al., 1991; Riis and Biggs, 2003; Sand-Jensen, 2008).
Our observations confirm that variations in water level regime lead to major temporal changes in environmental variables and in submersed macrophyte stands. Each flood period affected the vegetation differently. The low intensity flood period (2006) reduced macrophyte abundance in all habitats but not to such an extent that plants were unable to recover quickly afterwards. The 2007 extreme flood, however, almost completely eliminated above-ground plant biomass in all habitats. In the river sites plants took from five to eight months to start to regenerate, while in the lakes no substantial biomass increase was observed after the major flood up to the end of the study period (although by December 2008 Egeria growth was once again luxuriant in the lakes: Murphy and Thomaz, personal observation). When flood pulses occurred the water of the Parana´ River likely received substantial inputs of nutrients and suspended matter as evidenced by rises of phosphorus and nitrogen, as well as a decline in
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Table 3 Models yielded by stepwise regression analysis which explained H. verticillata and E. najas biomass (g DW m2) and net biomass increase rate (NBI; g DW m2 d1). The independent variables analyzed by the regression procedures were water temperature, light attenuation coefficient (kd), alkalinity, total phosphorus and total nitrogen, proportion of organic matter in the sediment (%OMsed), water level of the Parana´ River (mean of the last 30 days prior to the sampling survey) and biomass of H. verticillata and E. najas. Note: b is a measure of the relative contribution of each variable to the model. Dependent variable E. najas (g DW m n = 84
2
)
r2
F
p
Predictor
Coefficient
b
p
r2 change
0.291
10.95
<0.001
Intercept kd Temperature %OMsed
181.6 146.1 15.6 5.6
0.51 0.45 0.24
0.033 <0.001 <0.001 0.016
0.095 0.143 0.053
Intercept %OMsed kd Temperature
83.5 15.2 238.3 21.5
0.31 0.38 0.29
0.628 0.002 <0.001 0.003
0.204 0.074 0.074
H. verticillata (g DW m2) n = 84
0.352
E. najas NBI (g DW m2 d1) n = 92
0.195
2
H. verticillata NBI (g DW m n = 92
d
1
)
0.125
14.47
21.76
12.97
<0.001
<0.001
<0.001
Intercept WL
4.81 1.57
0.44
<0.001 <0.001
0.195
Intercept kd
3.83 3.39
0.35
<0.001 <0.001
0.125
Owing to the lack of %OMsed data for January, February and March 2006 (see Section 2) the regression analyses was firstly run without data from these surveys (n = 84). If %OMsed was not selected as a significant (p < 0.05) predictor then another analyses were run without %OMsed but with data from all surveys (n = 92 for NBI).
transparency. Moreover, elevated water flows and turbulence occasioned intense erosion and deposition processes especially during the major flood. Hence, floods probably impacted both species of Hydrocharitaceae (especially in 2007) through disturbance processes of sediment movement and plant scouring (uprooting), coupled with intense stress caused by low light availability. E. najas and H. verticillata both maximize light acquisition through stem elongation, forming dense and tall canopies, with biomass usually concentrated just below the water surface. Especially during stress periods caused by floods, light acquisition is likely a problem for both species in these riverine habitats, and they respond by growing longer. Following flood disturbances plants invested in shoot elongation prior to significant increases in biomass. Although both species are able to adapt photosynthesis to low light intensities, growth is maximized under higher light availability (Van et al., 1976; Tavechio and Thomaz, 2003). Moreover, the ability to elongate and maintain photosynthetic tissues near the water surface can give a competitive advantage to plants (Haller and Sutton, 1975; Van et al., 1999). Our study recorded biomass values of E. najas and H. verticillata much greater than observed elsewhere (e.g. Bowes et al., 1979; Spencer et al., 1994; Thomaz et al., 1999; Rybicki et al., 2001; Havens, 2003) which highlights the very high productivity of this subtropical riverine floodplain system. Macrophyte biomass peaked during periods of high water temperature and transparency and low-water levels. In the river sites, during the recovery process following flood disturbances the highest increases in biomass of both species occurred when temperature was rising from 24 to 28 8C (October–November 2006) and from 22 to 25 8C (September–October 2007). Although temperature was an important explanatory variable for the biomass of both species it is hard to determine how much this relationship reflects a direct effect of temperature upon plants growth or how much it expresses the effects of altered hydrological regimes on the Hydrocharitaceae stands, since water level regimes have a direct relationship with temperature in the Upper Parana´ system. While the temporal dynamics of the two target species were mainly related to variations in water level, transparency and temperature, sediment organic matter was also a strong predictor of spatial variation for biomass of both species, especially H. verticillata. Propagule availability was not the cause of this plant’s lack of success in colonizing lakes because fragments of Hydrilla were often observed in these habitats, brought in by the daily water exchange with the river channel. Moreover, periodical
surveys showed that up to December 2008 H. verticillata had not yet developed inside lakes (or had only extremely limited presence). Our results suggest that the high sediment organic content was likely hampering Hydrilla growth in the lakes. The negative impact of high sediment organic content upon Hydrilla has been shown experimentally by Barko and Smart (1983, 1986) who cited as one possible explanation the toxicity of compounds generated by anaerobic decomposition. More recently other authors have also demonstrated the effect of anoxia (favoured by organic matter decomposition) on the production of toxic compounds for aquatic plants (e.g. Moore et al., 1992; Pezeshki, 2001; Blokhina et al., 2003). While E. najas dominated the lakes it was likely suffering high competitive pressure from H. verticillata in the Parana´ River channel. The biggest E. najas development in the river sites occurred early in 2006 when H. verticillata was just starting its invasion. The competitive suppression of E. najas by H. verticillata was especially evident in R2 where the highest biomass of E. najas occurred while the invasive species was still absent. After that H. verticillata gradually increased to dominate the area while E. najas stands declined. However, E. najas showed a substantial recovery in both river sites after the major disturbance. These results indicate that major floods might hinder E. najas displacement by H. verticillata. Both species have high dispersal-regeneration ability through stem fragments (Cook and Lu¨o¨nd, 1982; Cook and UrmiKo¨nig, 1984; Rybicki et al., 2001; Thomaz et al., 2006) and since substantial sources of propagules exist plants can easily colonize areas opened up by floods (Combroux et al., 2002). The ability to regenerate after flood disturbance depends on the ecological traits of the species concerned, as well as the intensity of the impact from disturbance (Henry et al., 1996; Bornette et al., 2008). E. najas and H. verticillata demonstrated a substantial capacity for recovery following disturbances and started the regeneration process practically at the same time. After the larger flood event the regeneration process started earliest in the river site R2. The river site R1 was highly impacted by sediment deposition, which probably hampered regeneration. During the major flood, river waters overflowed lake banks intensely scouring vegetation. The scouring process was more intense in lake L1 due to its elongated form parallel to the river flow while lake L2 had a round shape and a narrower river connection channel which was likely to facilitate trapping of propagules. The longer time taken for biomass to recover in the lakes after the ENSO event suggests that these habitats are much less resilient to flood disturbances than are the river channel habitats. Constant propagule inflows via river
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water from reservoirs located upstream (which are densely colonized by submersed plants; Martins et al., 2008) may be important for the faster recovery seen in the river compared to its associated lakes. Regeneration inside the lakes was also probably delayed by a later recovery of water clarity compared with the river sites. For example, from June until December 2007 values of kd were significantly lower (t-test p < 0.001) in the river (mean 0.66 0.07 m1) than in the lakes (mean 1.15 0.06 m1). Some characteristics of H. verticillata compared to E. najas might confer an advantage of the invasive over the native species in regard to its higher growth rates. For example, E. najas carbohydrates are mainly stored in the shoots while H. verticillata can allocate reserves within a developed root system as well as in underground turions (Netherland, 1997; Owens and Madsen, 1998). Carbohydrate storage in below-ground structures is also a plausible explanation for the higher growth achieved by H. verticillata in 2007 compared with 2006. In 2006 H. verticillata apparently invested in its below-ground parts and in ‘‘resistance’’ structures that cannot be uprooted easily, being able to use these reserves to produce photosynthetic structures after the major disturbance and thus helping its fast recovery. Acknowledgements The first author thanks the Brazilian Council of Research (CNPq) and the Coordenadoria de Aperfeic¸oamento de Pessoal de Nı´vel Superior (CAPES) for funding his Ph.D. course. We are also grateful to Msc. Ma´rcio Silveira for helping with field work and laboratory analysis. S.M. Thomaz is a Productivity Researcher from CNPq and acknowledges this agency for constant funding. Survey work was partially funded by CNPq though the Long Term Ecological Research Program (site number 6). References Agostinho, A.A., Gomes, L.C., Verissimo, S., Okada, E.K., 2004. Flood regime, dam regulation and fish in the Upper Parana River: effects on assemblage attributes, reproduction and recruitment. Rev. Fish Biol. Fish. 14, 11–19. Barko, J.W., Smart, R.M., 1981. Comparative influences of light and temperature on the growth and metabolism of selected submersed freshwater macrophytes. Ecol. Monogr. 51, 219–235. Barko, J.W., Smart, R.M., 1983. Effects of organic matter additions to sediment of the growth of aquatic plants. J. Ecol. 71, 161–175. Barko, J.W., Smart, R.M., 1986. Sediment regulates mechanisms of growth limitation in submersed macrophytes. Ecology 67, 1328–1340. Barrat-Segretain, M., Bornette, G., Hering-Vilas-Boˆas, A., 1998. Comparative abilities of vegetative regeneration among aquatic plants growing in disturbed habitats. Aquat. Bot. 60, 201–211. Bini, L.M., Thomaz, S.M., 2005. Prediction of Egeria najas and Egeria densa accurrence in a large subtropical reservoir (Itaipu Reservoir, Brazil-Paraguay). Aquat. Bot. 83, 227–238. Blokhina, O., Virolainen, E., Fagerstedt, K.V., 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. 91, 179–194. Bornette, G., Amoros, C., Castella, C., Beffy, J.L., 1994. Succession and fluctuation in the aquatic vegetation of two former Rhoˆne River channels. Vegetatio 110, 171– 184. Bornette, G., Tabacchi, E., Hupp, C., Puijalon, S., Rostan, C., 2008. A model of plant strategies in fluvial hydrosystems. Freshwater Biol. 53, 1692–1705. Bowes, G., Holaday, S., Haller, W.T., 1979. Seasonal variation in the biomass, tuber density, and photosynthetic metabolism of Hydrilla in three Florida lakes. J. Aquat. Plant Manage. 15, 32–35. Chambers, P.A., Prepas, E.E., Hamilton, H.R., Bothwell, M.L., 1991. Current velocity and its effect on aquatic macrophytes in flowing waters. Ecol. Appl. 1, 249–257. Carmouze, J.P., 1994. O metabolismo dos ecossistemas aqua´ticos. Edgard Blu¨cher/ SBL/FABESP, Sa˜o Paulo. Combroux, I.C.S., Bornette, G., Amoros, C., 2002. Plant regenerative strategies after a major disturbance: the case of a riverine wetland restoration. Wetlands 22, 234–246. Connell, J.H., 1978. Diversity in tropical rain forest and coral reefs. Science 199, 1302–1310. Cook, C.D.K., Lu¨o¨nd, R., 1982. A revision of the genus Hydrilla (Hydrocharitaceae). Aquat. Bot. 13, 485–504. Cook, C.D.K., Urmi-Ko¨nig, K., 1984. A revision of the genus Egeria (Hydrocharitaceae). Aquat. Bot. 19, 73–96.
47
Golterman, H.L., Clymo, R.S., Ohmstad, M.M., 1978. Methods for Physical and Chemical Analysis of Fresh Waters. Blackwell Scientific Publications, Oxford. Haller, W.T., Sutton, D.L., 1975. Community structure and competition between Hydrilla and Vallisneria. J. Aquat. Plant Manage. 13, 48–50. Havens, K.E., 2003. Submersed aquatic vegetation correlation with depth and light attenuating materials in a shallow subtropical lake. Hydrobiologia 493, 173– 186. Henry, C.P., Amoros, C., Bornette, G., 1996. Species traits and recolonization process after flood disturbances in riverine macrophytes. Vegetatio 122, 13–27. Hershner, C., Havens, K.J., 2008. Managing invasive aquatic plants in a changing system: strategic consideration of ecosystem services. Conserv. Biol. 22, 544– 550. Junk, W.J., Bayley, P.B., Sparks, R.E., 1989. The flood pulse concept in river-floodplain systems. Can. Spec. Publ. Fish. Aquat. Sci. 106, 110–127. Kahara, S.N., Vermaat, J.E., 2003. The effect of alkalinity on photosynthesis-light curves and inorganic carbon extraction capacity of freshwater macrophytes. Aquat. Bot. 75, 217–227. Kirk, J.T.O., 1994. Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Cambridge. Madsen, J.D., Smith, D.H., 1999. Vegetative spread of dioecious Hydrilla colonies in experimental pounds. J. Aquat. Plant Manage. 37, 25–29. Maltchik, L., Rolon, A.S., Schott, P., 2007. Effects of hydrological variation on the aquatic plant community in a floodplain palustrine wetland of southern Brazil. Limnology 8, 23–28. Martins, D., Marchi, S.R., Costa, N.V., 2005. Estudo da movimentac¸a˜o de plantas aqua´ticas imersas presentes no reservato´rio da UHE Eng. Souza Dias – Jupia´ Planta Daninha 23, 351–358. Martins, D., Costa, N.V., Terra, M.A., Marchi, S.R., 2008. Characterization of the aquatic plant communities of 18 reservoirs of five watersheds in Sa˜ol Paulo, Brazil. Planta Daninha 26, 17–32. Mony, C., Koschnick, T.J., Haller, W.T., Muller, S., 2007. Competition between two invasive (Hydrocharitaceae Hydrilla verticillata (L.f.) (Royle) and Egeria densa (Planch)) as influenced by sediment fertility and season. Aquat. Bot. 86, 236– 242. Moore, P.A., Reddy, K.R., Graetz, D.A., 1992. Water quality—nutrient transformations in sediments as influenced by oxygen supply. J. Environ. Qual. 21, 387– 393. Mullin, B.H., Anderson, L.W.J., DiTomaso, J.M., Eplee, R.E., Getsinger, K.D., 2000. Invasive plant species. CAST 13, 1–18. Murphy, K.J., 1988. Aquatic weed problems and their management: a review. I. The worldwide scale of the aquatic weed problem. Crop Prot. 7, 232–248. Murphy, K.J., Pieterse, A.H., 1990. Present status and prospects of integrated control of aquatic weeds. In: Pieterse, A.H., Murphy, K.J. (Eds.), The Ecology and Management of Nuisance Aquatic Vegetation. Oxford Publications, New York, pp. 222–227. Neiff, J.J., 1990. Ideas para la interpretacion ecologica del Parana´. Interciencia 15, 424–441. Netherland, M.D., 1997. Turion ecology of Hydrilla. J. Aquat. Plant Manage. 35, 1–10. Owens, C.S., Madsen, J.D., 1998. Phenological studies of carbohydrate allocation in Hydrilla. J. Aquat. Plant Manage. 36, 40–44. Padial, A.A., Thomaz, S.M., 2008. Prediction of the light attenuation coefficient through the Secchi disk depth: empirical modeling in two large Neotropical ecosystems. Limnology 9, 143–151. Pezeshki, S.R., 2001. Wetland plant responses to soil flooding. Environ. Exp. Bot. 46, 299–312. Pierini, S.A., Thomaz, S.M., 2004. Effects of inorganic carbon source on photosynthetic rates of Egeria najas Planchon and Egeria densa Planchon (Hydrocharitaceae). Aquat. Bot. 78, 135–146. Riis, T., Biggs, B.J.F., 2003. Hydrologic and hydraulic control of macrophyte establishment and performance in streams. Limnol. Oceanogr. 48, 1488– 1497. Rybicki, N.B., McFarland, D.G., Ruhl, H.A., Reel, J.T., Barko, J.W., 2001. Investigations of the availability and survival of submersed aquatic vegetation propagules in the tidal Potamic River. Estuaries 24, 407–427. Sand-Jensen, K., 2008. Drag forces on common plant species in temperate streams: consequences of morphology, velocity and biomass. Hydrobiologia 610, 307– 319. Santos, A.M., Thomaz, S.M., 2007. Aquatic macrophytes diversity in lagoons of a tropical floodplain: the role of connectivity and water level. Aust. Ecol. 32, 177– 190. Souza-Filho, E.E., Comunello, E., Rocha, P.C., 2004a. Flood extension in the BaiaCurutuba-Ivinheima complex of the Parana River Floodplain. In: Agostinho, A.A., Rodrigues, L., Gomes, L.C., Thomaz, S.M., Miranda, L.A. (Eds.), Structure and Functioning of the Parana´ River and its Floodplain: LTER – Site 6 – (PELD – Sı´tio 6). Eduem, Maringa´, pp. 19–24. Souza-Filho, E.E., Rocha, P.C., Comunello, E., Stevaux, J.C., 2004b. Effects of the Porto Primavera Dam on physical environment of the downstream floodplain. In: Thomaz, S.M., Agostinho, A.A., Hahn, N.S. (Eds.), The Upper Parana´ River and its Floodplain: Physical Aspects, Ecology and Conservation. Blackhuys, Liden, pp. 55–74. Spencer, W.E., Teeri, J., Wetzel, R.G., 1994. Acclimation of photosynthetic phenotype to environmental heterogeneity. Ecology 75, 301–314. Tavechio, W.L.G., Thomaz, S.M., 2003. Effects of light on the growth of Egeria najas Planchon. Braz. Arch. Biol. Technol. 46, 203–209. Thomaz, S.M., Bini, L.M., 1999. A expansa˜o das macro´fitas aqua´ticas e implicac¸o˜es para o manejo de reservato´rios: um estudo na represa de Itaipu. In: Henry, R.
48
W.T.Z. Sousa et al. / Aquatic Botany 92 (2010) 40–48
(Ed.), Ecologia de Reservato´rios: Estrutura, Func¸a˜o e Aspectos Sociais. FAPESP/ Fundibio, Botucatu, pp. 599–625. Thomaz, S.M., Bini, L.M., Souza, M.C., Kita, K.K., Camargo, A.F.M., 1999. Aquatic macrophytes of Itaipu reservoir, Brazil: surveys of species and ecological considerations. Braz. Arch. Biol. Technol. 42, 15–22. Thomaz, S.M., Pagioro, T.A., Bini, L.M., Murphy, K.J., 2006. Effect of reservoir drawdown on biomass of three species of aquatic macrophytes in a large sub-tropical reservoir (Itaipu, Brazil). Hydrobiologia 570, 53–59. Thomaz, S.M., Bini, L.M., Bozelli, R.L., 2007. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia 579, 1–13. Thomaz, S.M., Carvalho, P., Padial, A.A., Kobayashi, J.T., 2009. Macrophytes in the Upper Parana´ River floodplain: long term patterns over large spatial scales. Braz. J. Biol. 69, 617–625. Van, T.K., Haller, W.T., Bowes, G., 1976. Comparison of the photosynthetic characteristics of three submersed aquatic plants. Plant Physiol. 58, 761–768.
Van, T.K., Wheeler, G.S., Center, T.D., 1999. Competition between Hydrilla verticillata and Vallisneria americana as influenced by soil fertility. Aquat. Bot. 62, 225–233. Van Geest, G.J., Wolters, H., Roozen, F.C.J.M., Coops, H., Roijackers, R.M.M., Buijse, A.D., Scheffer, M., 2005. Water-level fluctuations affect macrophyte richness in floodplain lakes. Hydrobiologia 539, 239–248. Wang, J., Yu, D., Xiong, W., Han, Y., 2008. Above- and belowground competition between two submersed macrophytes. Hydrobiologia 607, 113–122. Ward, J.V., Tockner, K., Arscott, D.B., Claret, C., 2002. Riverine landscape diversity. Freshwater Biol. 47, 517–539. Wingfield, R., Murphy, K.J., Gaywood, M., 2006. Assessing and predicting the success of Najas flexilis (Willd.) Rostk. & Schimidt, a rare European aquatic macrophyte, in relation to lake environmental conditions. Hydrobiologia 570, 79–86. Zagatto, E.A.G., Jacintho, A.O., Reis, B.F., Krug, F.J., Bergamin, H., Pessenda, L.C., Mortatti, R.J., Gine´, M.F., 1981. Manual de ana´lises de plantas empregando sistemas de injec¸a˜o em fluxo. USP, Piracicaba.