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Hydrobiologia https://doi.org/10.1007/s10750-018-3607-y

PHYTOPLANKTON & BIOTIC INTERACTIONS

Phytoplankton species interactions and invasion by Ceratium furcoides are influenced by extreme drought and water-hyacinth removal in a shallow tropical reservoir Luciane Oliveira Crossetti . Denise de Campos Bicudo . Luis Mauricio Bini . Renato Bolson Dala-Corte . Carla Ferragut . Carlos Eduardo de Mattos Bicudo

Received: 6 December 2017 / Revised: 13 March 2018 / Accepted: 30 March 2018 Ó Springer International Publishing AG, part of Springer Nature 2018

Abstract This study explored the interactions of phytoplankton species during the invasion of Ceratium furcoides and the environmental variables that contributed to its establishment and ecological success in a shallow eutrophic reservoir (Garc¸as Reservoir, southeast Brazil), which has been monitored monthly for 20 years (1997–2017). The Ceratium furcoides invasion in September 2014 was preceded by disturbance events (macrophyte removal and a historical drought period), which disrupted the dominance of cyanobacteria by modifying resource availability

Guest editors: Hugo Sarmento, Irina Izaguirre, Vanessa Becker & Vera L. M. Huszar / Phytoplankton and its Biotic Interactions L. O. Crossetti (&) Departamento de Ecologia, Instituto de Biocieˆncias, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil e-mail: [email protected] D. C. Bicudo  C. Ferragut  C. E. de Mattos Bicudo Departamento de Ecologia, Instituto de Botaˆnica, Sa˜o Paulo, SP, Brazil L. M. Bini Departamento de Ecologia, Instituto de Cieˆncias Biolo´gicas, Universidade Federal de Goia´s, Goiaˆnia, GO, Brazil R. B. Dala-Corte Programa de Po´s-Graduac¸a˜o em Biodiversidade Animal, Universidade Federal de Goia´s, Goiaˆnia, GO, Brazil

(high water transparency and soluble reactive phosphorus concentrations) and recruiting other species. Ceratium blooms at the water surface were preceded by high abundance near the bottom, suggesting the importance of the propagule bank. However, the pattern of Ceratium-Microcystis coexistence that is usually recorded in temperate lakes was not observed. Instead, Ceratium replaced Cylindrospermopsis raciborskii in mixing periods with high light and nitrogen availabilities, significantly influencing the abundance of Trachelomonas spp. Flagellated forms became dominant in the Garc¸as Reservoir, due to the higher water transparency and relatively lower water-column stability, and alternative states between CeratiumTrachelomonas in mixing periods and MicrocystisCryptomonas in stratified periods have been repeated. Since then, cyanobacterial dominance ceased, and the ‘‘skillful’’ Ceratium apparently has come to stay, influencing interactions among phytoplankton species. Keywords Biotic interaction  Phosphorus  Water transparency  Flagellates

Introduction The structure of freshwater communities is the result not only of abiotic variations, but also of biotic interactions (De Bernardi, 1981). For phytoplankton

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communities, ecological studies have shown that the structural and dynamic responses are related at some level to inter- or intraspecific interactions, from the questions driven by the Paradox of the Plankton (Hutchinson, 1961) to studies on the role of disturbances (Sommer et al., 1993) and the susceptibility of steady states in the phytoplankton (Naselli-Flores et al., 2003). Among the best-known outcomes of interactions among phytoplankton species is competitive exclusion, as demonstrated by Tilman et al. (1981). They showed that Ulnaria ulna (Nitzsch) Compe`re (former Synedra ulna (Nitzsch) Ehrenberg) competitively excluded Asterionella formosa Hassall by maintaining the concentrations of common resources at low levels. Even though this example is often found in ecology textbooks, identifying and understanding species interactions in phytoplankton in natural communities may be challenging, especially under recurrent scenarios of many species coexisting in a single waterbody and usually requiring the same resources (Hutchinson, 1961). Phytoplankton organisms possess several mechanisms to avoid loss processes (Reynolds, 1984). Some organisms have evolved vertical migration abilities, special strategies for nutrient uptake (e.g., luxury consumption, nitrogen fixing), and size differences, among others, as mechanisms to reduce or optimize negative interactions such as predation or competition (De Bernardi, 1981). So, the role of environmental gradients in selecting traits cannot be ignored, since environmental disturbances reset phytoplankton succession (Sommer et al., 1993), making it easier, for instance, to observe biological interactions between organisms (De Bernardi, 1981). The susceptibility of an environment to the invasion of non-native species can be determined by the availability of propagules and the ecological abilities of the invader, besides the fluctuation in resource availability (Davis et al., 2000). For freshwater phytoplankton, geographic distribution patterns exist and invasions into new areas are ongoing (Padisa´k et al., 2016). The increasingly frequent invasions by phytoplankton species have demonstrated the extent of the dispersal processes of this group (see Padisa´k, 1997; Korneva, 2014; Meichtry de Zaburlı´n et al., 2016; Vidakovic´ et al., 2016). Likewise, relationships between phytoplankton invasion and loss of diversity of native species, as well as the effects of invasive-

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species dominance on the entire ecosystem as a major organizing force have been examined (Padisa´k et al., 2010; Selmeczy et al., 2016). Invasions by members of the genus Ceratium (Dinophyta) have recently occurred in South American freshwater systems, for example in Chile (Almanza et al., 2016), Bolivia (Morales, 2016), Argentina (Donagh et al., 2005; Meichtry de Zaburlı´n et al., 2014), and Colombia (Gil et al., 2012). In Brazil, the establishment of Ceratium furcoides (Levander) Langhans has gained the attention of many aquatic ecologists, being recently recorded in several aquatic ecosystems, such as water-supply reservoirs (Matsumura-Tundisi et al., 2010; Nishimura et al., 2015; Cavalcante et al., 2016), fish-farm lakes (Campanelli et al., 2017), floodplain lakes and rivers (Jati et al., 2014), hydroelectric reservoirs (Santos-Wisniewski et al., 2007; Silva et al., 2012; Cassol et al., 2014), rivers and reservoirs of the semi-arid northeastern region (Oliveira et al., 2011), and high-altitude lakes (Moreira et al., 2015). Ceratium furcoides and Ceratium hirundinella (O. F. Mu¨ller) Dujardin, which are typically found in the northern hemisphere (the latter more commonly), are ecologically similar, as discussed by Gil et al. (2012). Ceratium species are usually more abundant in stratified water bodies during the summer in temperate lakes with low nutrient concentrations (Dokulil & Teubner, 2003), with populations declining during the beginning of the mixing period in autumn (Lindstro¨m, 1992). They may also occur during the onset of mixing (Naselli-Flores & Barone, 2003). Changes in Ceratium density may be insensitive to variations in trophic conditions (Padisa´k, 1985). Low light and low temperature seem to limit Ceratium development, making it nearly absent during winter in temperate lakes (Pe´rez-Martı´nez & Sa´nches-Castillo, 2002). Ceratium species are S-strategists (K-selected species), dealing effectively with limiting nutrient resources, either by exploiting alternative sources (mixotrophy) or by using motility, migrating over large vertical distances to avoid light constraints or to access the more nutrient-rich deep water layers (Reynolds, 2006). Except for mixotrophy, the cyanobacteria Microcystis also shows the same features, and it is not by chance that these species often coexist in the summer epilimnia of eutrophic temperate lakes, comprising functional group LM of Reynolds et al. (2002). This functional group may

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contribute to phytoplankton steady-states (NaselliFlores & Barone, 2003; Dokulil & Teubner, 2003), by using their life strategies to outcompete other, lessspecialized species. However, one may wonder whether these interactions classically recorded in temperate freshwaters will also occur in ecosystems where Ceratium species are considered invasive, such as the highly diverse tropical lakes and reservoirs of Brazil. Invasions by planktonic algal species are poorly documented, one of the reasons being the lack of reliable historical data (Padisa´k et al., 2016). Therefore, studies of the interactions among phytoplankton species during an invasion process in natural communities are scarce. The present study explored the interactions of phytoplankton species during the invasion of Ceratium furcoides in a tropical shallow eutrophic reservoir (Garc¸as Reservoir, southeastern Brazil), which has been monitored monthly for more than 20 years uninterruptedly and where cyanobacteria (mainly Microcystis aeruginosa (Ku¨tzing) Ku¨tzing and Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju) have historically dominated (Bicudo et al., 2007). For this study, the main driving questions were as follows: (i) what environmental variables contributed most to the establishment and the ecological success of Ceratium furcoides? and (ii) what phytoplankton species interactions could be observed during the invasion process of C. furcoides?

Materials and methods Study area Garc¸as Reservoir (23°380 S, 046°370 W) is located in the Parque Estadual das Fontes do Ipiranga, which is a protected area of Atlantic Rain Forest within the municipality of Sa˜o Paulo, in southeastern Brazil (Fig. 1). The regional climate is tropical of altitude (Conti & Furlan, 2003) and winds are usually of low intensity (\ 2.5 m s-1). Higher precipitation levels usually occur from October to March (rainy period) and the lower levels may be registered from April to September (dry period). Garc¸as Reservoir is a shallow (maximum depth of 4.7 m), discontinuous warm polymictic reservoir (Lewis, 1983), with a surface area of 88 156 m2, volume 188 785 m3, maximum length 512 m, maximum width 319.5 m and mean

theoretical residence time of 71 days (Bicudo et al., 2002). The eutrophication history of Garc¸as Reservoir has been monitored monthly since January 1997. The eutrophication process was caused mainly by the input of untreated sewage from the tributary with drainage from the city zoo. A drastic increase of allochthonous nutrients (N, P) led to the development of Eichhornia crassipes, which covered 40–70% of the reservoir surface from April 1998 to August 1999 (TP = 74.7 lg l-1). The removal of the macrophytes due to mosquito infestation (Mansonia sp.) in September 1999 was considered an ‘‘abrupt permanent impact,’’ which caused cyanobacterial blooms, especially Microcystis spp., to intensify and persist. This was most likely due to an increase in water-column thermal stability, changes in internal P cycling, and feedback mechanisms (Bicudo et al., 2007). During that period, a small macrophyte stand, covering about 10% of the reservoir surface, was maintained with the aid of metal frames and wires, near the inflow zone (Fig. 1). This situation continued until the end of 2007, when a secondary sewage-treatment plant was installed in the city zoo tributary. In 2014, the rainy season in southeast Brazil was atypically dry (Marengo et al., 2015). In that year, this region faced one of its worst recorded droughts, mainly in Sa˜o Paulo State (Soriano et al., 2016). In the same year (July 2014), part of the macrophyte stand was removed, and as a result the sediment was vigorously stirred. In the present study, the drought event and the macrophyte-stand management were considered disturbances, following the concept of Borics et al. (2013): ‘‘If the frequency of the event enables the variable to reach a dynamic equilibrium which might be exhibited without this event, then the event (plus its responses) is a disturbance for the system’’. Abiotic and biotic variables Sampling was conducted monthly from January 2008 to September 2017, at five depths in the deepest part of the reservoir (Fig. 1). Water samples were collected with a van Dorn bottle. Water temperature, pH, and conductivity were measured in the field using a probe (Yellow Springs Instrument). Water transparency was determined using a Secchi disk. The relative watercolumn stability (RWCS) was calculated according to

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Fig. 1 Map showing the location of the city of Sa˜o Paulo metropolitan urban region (gray) and municipality, and the reserve of Parque Estadual das Fontes do Ipiranga (PEFI).

Enlarged map of Garc¸as Reservoir and its inflows (numbered arrows), outlet and sampling station (asterisk) Reproduced with reference from Bicudo et al. (2007)

Padisa´k et al. (2003), based on the thermal profile. The mixing zone (Zmix) was estimated according to Reynolds (1984) and the euphotic zone (Zeu) was determined based on Cole (1983). Dissolved oxygen (DO) (Winkler modified by Golterman et al., 1978), alkalinity (Golterman & Clymo, 1971), free CO2, HCO3-, and CO3- (Mackereth et al., 1978), soluble

reactive phosphorus (SRP) and total dissolved phosphorus (TDP) (Strickland & Parsons, 1960), total phosphorus (TP) (Valderrama, 1981), nitrite (NO2-) and nitrate (NO3-) (Mackereth et al., 1978), ammonium (NH4?) (Solorzano, 1969), total nitrogen (TN) (Valderrama, 1981), and soluble reactive silica (SRS) (Golterman et al., 1978) were also determined on the

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day of sampling. Dissolved inorganic nitrogen (DIN) was estimated by the addition of nitrite, nitrate, and ammonium concentrations. Chlorophyll a concentration, corrected for phaeophytin, was determined according to Sartory & Grobbelaar (1984). Phytoplankton quantification followed Utermo¨hl (1958). Biomass was estimated by biovolume calculation (mm3 l-1), using geometric approximations (Hillebrand et al., 1999). Species were sorted into functional groups according to Reynolds et al. (2002) and Padisa´k et al. (2009). Data analysis A correlation-based principal components analysis (PCA) was performed, using PC-Ord 6 (McCune & Mefford, 2011) to assess the main trends of the environmental variables over time. The relationships among the disturbance, physical and chemical variables, as well as the biological variables (phytoplankton genera) were investigated using a structural equation modeling (SEM; Grace et al., 2015). These relationships were defined a priori in a global path model based on theoretical predictions. Specifically, the variables included in this model and their respective categories were as follows: (1) disturbance (drought and macrophyte [water hyacinth] removal); (2) physical (water transparency and RWCS); (3) nutrients (DIN, TN:TP, SRP); and (4) biological (Ceratium furcoides—functional group LO, Cylindrospermopsis raciborskii—functional group SN, Microcystis aeruginosa—functional group M, Cryptomonas spp.—functional group Y, Trachelomonas spp.—functional group W2). Based on the global conceptual path model, six other models were derived, including different variables to represent nutrients and chemical variables. A posteriori, three other relationships not predicted in our conceptual model were added because they proved to be important for model goodness-of-fit (i.e., Cryptomonas predicted by drought; Cylindrospermopsis predicted by water hyacinth removal; and Cryptomonas predicted by water hyacinth removal). To fit and test these models, we carried out the piecewiseSEM analysis (Lefcheck, 2016). This analysis was appropriate because it allowed us to control for temporal autocorrelation in the data, which was done by specifying months nested in years as random-effect variables. Therefore, each relationship within the path

models was fitted to a linear mixed effect model using the package nlme (Pinheiro et al., 2017), for R (R Core Team, 2017). Afterwards, the goodness-of-fit of each model was evaluated using Fisher’s C statistic (Shipley, 2013), implemented for R by Lefcheck (2016). The best model was selected by using informationtheory methods (Burnham & Anderson, 2002). The effect size of each variable in the SEM models was calculated by the standardized regression coefficient (std-b) between pairs of variables, as provided by the piecewiseSEM analysis (Lefcheck, 2016). The indirect effects (IE) of disturbance factors on phytoplankton genera were calculated by multiplying significant (P B 0.05) standardized coefficients from each disturbance to the phytoplankton-species response variables (Legendre & Legendre, 2012). The marginal R2 was also provided for each response variable in the selected SEM model, which corresponds to the explanation of the fixed-effect variables exclusively.

Results Environmental temporal variation The lowest precipitation amounts were recorded in June, July, and August 2014 (dry season) (Fig. 2A). RWCS followed seasonal changes, with lower values in the winter months and higher values in summer periods, except for the values observed in the summer after the drought event (2014), especially in 2015–2016. The lowest RWCS observed in that period (January 2016) was about 14 (Fig. 2B). Water transparency increased after the disturbance events. The highest transparencies were usually recorded during the mixing periods, reaching 1.3 m in July 2016, and 1.0 m in September 2014 (Fig. 2C), when the highest value of the Zeu:Zmix ratio (3.0) was also observed (Fig. 2D). Due to the high values of Zeu observed after the disturbances (Table 1), the Zeu:Zmix ratio also increased, indicating high light availability during the mixing periods. Higher concentrations of DO were recorded in the deeper layers than before the disturbances. Soon after the disturbance events, SRP concentrations peaked (51.6 lg l-1, in August 2014) (Fig. 2E; Table 1), when low levels of chlorophyll a (19 lg l-1) and an increase in water transparency (0.7 m) were observed.

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Hydrobiologia Fig. 2 Precipitation (mm, A); relative water-column stability, RWCS (B); transparency (m, C); Zeu:Zmix, ratio (D); and soluble reactive phosphorus, SRP (E) in Garc¸as Reservoir, from 2008 to 2017

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Hydrobiologia Table 1 Minimum (min), maximum (max), mean values, and standard deviation (SD) of abiotic and biological variables in Garc¸as Reservoir, before the disturbance events (Jan 2008– Variables

May 2014), in rainy (n = 39) and dry (n = 38) periods, and afterward (Jun 2014–Sept 2017), regarding Ceratium absence (rainy period; n = 21) and presence (dry period; n = 19)

Jan 2008–May 2014

Jun 2014–Sept 2017

Before disturbance

After disturbance

Rainy period

Dry period

Min–max

Min–max

Mean-SD

Mean-SD

Ceratium absent

Ceratium present

Min–max

Min–Max

3–368

Mean-SD

Mean-SD

Precipitation (mm)

72–653

214 ± 116

0.4–203

74 ± 55

Water Temperature (°C) RWCS

17–27

24 ± 2

15–23

19 ± 2

0–204

114 ± 58

0–95

32 ± 27

0–177

78 ± 49

0–129

41 ± 42

Transparency (m)

0.1–0.5

0.3 ± 0.1

0.1–0.9

0.4 ± 0.2

0.1–0.8

0.5 ± 0.2

0.3–1.3

0.7 ± 0.2

16–28

158 ± 106

2–218

96 ± 73

23 ± 3.0

15–24.3

19 ± 3

Zeu (m)

0.3–1.6

0.8 ± 0.3

0.2–2.7

1.1 ± 0.6

0.3–2.5

1.4 ± 0.5

0.8–4.0

2.1 ± 0.7

Zmix (m)

1.0–4.0

1.6 ± 0.9

0.5–4.0

2.0 ± 1.2

1.0–4.0

1.9 ± 1.1

1.0–4.0

2.5 ± 1.3

Zeu/Zmix

0.1–1.6

0.7 ± 0.4

0.1–2.7

0.7 ± 0.6

0.2–2.0

0.9 ± 0.5

0.4–3.0

1.1 ± 0.8

Chlorophyll a (lg l-1)

28–453

160 ± 100

29–472

129 ± 96

19–204

73 ± 48

21–279

106 ± 70

Conductivity (lS cm-1)

2–370

190 ± 84

68–600

216 ± 92

146–467

258 ± 100

181–454

241 ± 68 7.1 ± 1.2

pH

2.3–9.8

7.7 ± 1.6

4.5–9.8

7.2 ± 1.3

4.6–10.2

7.6 ± 1.7

5.0–9.2

DO (mg l-1)

2.9–14.9

8.0 ± 3.0

2.8–15.1

8.2 ± 2.7

4.7–15.7

8.9 ± 2.9

4.9–14.2

8.5 ± 2.2

NH4? (lg l-1)

10–1109

237 ± 309

20–2690

957 ± 705

6–2264

364 ± 637

20–2210

857 ± 602

NO2- (lg l-1)

5–38

12 ± 10

5–86

23 ± 18

5–35

10 ± 9

5–87

37 ± 21

NO3- (lg l-1)

8–697

90 ± 158

8–820

226 ± 176

3–269

60 ± 75

8–613

199 ± 137

340 ± 369

44–2903

1205 ± 707

14–2376

434 ± 686

33–2340

1093 ± 644

3499 ± 1394

409–6602

2264 ± 1564

891–5171

2644 ± 1198 6.4 ± 5.4

DIN (lg l-1)

23–1132

TN (lg l-1)

182–5327

SRP (lg l-1)

4.0–14.1

5.5 ± 2.4

4.0–17.2

6.4 ± 3.4

4.0–51.6

9.7 ± 11.7

2.1–26.3

TDP (lg l-1)

3–47

21 ± 10

7–88

27 ± 16

7–41

21 ± 10

14–58

29 ± 14

TP (lg l-1)

41–226

126 ± 39

63–274

121 ± 47

43–185

99 ± 37

50–149

100 ± 23

NT:PT (molar) SRSi (mg l-1)

2–93 0.4–10.1

40 ± 21 3.1 ± 2.1

14–140 1.9–4.5

73 ± 36 2.9 ± 0.6

5–275 0.4–4.1

59 ± 62 2.2 ± 1.0

24–138 0.7–3.8

61 ± 27 2.5 ± 0.8

free CO2 (mg l-1)

0.1–138

38 ± 30

0.2–485

58 ± 79

0.0–40

7 ± 12

0.1–51

13 ± 18

HCO3(mg l-1)

3–141

49 ± 19

29–66

51 ± 8

33–72

52 ± 12

23–67

53 ± 11

0.0–0.0

0.0 ± 0.0

0.0–0.0

0.0 ± 0.0

0.0–0.0

0.0 ± 0.0

1.8–213.1

30.7 ± 50.5

Ceratium (mm3 l-1)

2150 ± 1137 1017–6349

M (mm3 l-1)

0–88.9

8.5 ± 20.0

0.0–23.9

1.0 ± 3.9

0.0–30.7

3.9 ± 7.3

0.0–30.7

5.1 ± 9.4

SN (mm3 l-1)

0.1–85.5

24.5 ± 23.4

0.0–64.4

19.9 ± 18.3

0.0–66.9

5.3 ± 15.0

0.0–27.7

1.9 ± 6.4

W2 (mm3 l-1)

0.0–3.5

0.6 ± 0.7

0.0–6.6

0.9 ± 1.3

0.0–3.3

0.5 ± 0.9

0.0–16.6

3.0 ± 4.4

Y (mm3 l-1)

0.0–7.0

0.9 ± 1.4

0.0–11.1

1.2 ± 2.1

0.0–36.6

4.3 ± 8.3

0.0–31.5

3.7 ± 7.6

Total biomass (mm3 l-1)

7.9–106.2

38.5 ± 24.9

1.6–76.2

24.1 ± 19.6

19.2 ± 17.8

7.5–231.3

47.3 ± 52.4

2.0–74

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At the same time, higher concentrations of DIN (2375 lg l-1), mainly influenced by higher ammonium concentrations (2264 lg l-1), were recorded (Table 1), as well as a decrease in the NT:PT ratio, which reached 10.5 in September 2014. Summarizing the analysis of abiotic variables, the first two PCA axes explained 40.4% of the total variance (Fig. 3). RWCS (r = –0.80), temperature (- 0.78), ammonium (0.75), and TN:TP ratio (0.70) were the most important variables on the first axis. Zeu:Zmix (0.83), Zmix (- 0.50), and water transparency (0.49) were the most important variables on the second axis. Most of the sampling units before the disturbance events were associated with the higher values of RWCS, temperature, TP, and chlorophyll a. Conversely, the higher values of water transparency, Zeu:Zmix and NT:PT, as well as higher concentrations of ammonium and nitrate characterized the period after the disturbance and with Ceratium present (Fig. 3).

Phytoplankton temporal variation From 2008 up to 2017, 134 phytoplankton species were identified. Total biomass reached 106 mm3 l-1 before the disturbance events (December 2011), mainly represented by Cyanobacteria (104 mm3 l-1) (Fig. 4A). In that period, the dominance of bluegreens was due mainly to functional group SN (Cylindrospermopsis raciborskii), and a low contribution of codon M (Microcystis aeruginosa, mainly) in the summer of 2012, reaching 88.9 mm3 l-1 (Fig. 5B). Group Y (Cryptomonas spp.) dominated in July 2011 (11.1 mm3 l-1), contributing more than 95% of the total biomass (Fig. 4A). This increase in dominance coincided with increases in water transparency (0.9 m), SRP (17.2 lg l-1), nitrate (415.8 lg l-1), and TN and TP concentrations (6313 and 127.8 lg l-1, respectively). Ceratium furcoides was first recorded in Garc¸as Reservoir in September 2014, with 12.3 lg l-1 (51%

Fig. 3 PCA biplot of limnological variables at sub-surface of Garc¸as Reservoir, from 2008 to 2017. The variables presented are those with r C 0.2

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Hydrobiologia Fig. 4 Relative biomass (%) of Ceratium furcoides, Cyanobacteria and other phytoplankton species (A) and main functional groups (B) in Garc¸as Reservoir, from 2008 to 2017

Fig. 5 Relative biomass (%) of main functional groups at the surface and at the bottom of Garc¸as Reservoir, from January to September 2017

of the total biomass), together with groups Y (46% of the total biomass) and W2 (Trachelomonas spp., 2% of the total biomass) (Fig. 4B). In that month, high transparency (1.0 m) and decreases in the NT:PT ratio (from 275.4 to 77.9) and SRP concentration (26.3 lg l-1) were observed. Since then, C. furcoides occurrence was recorded in winter periods (dry period), with higher Zeu, Zeu:Zmix, lower RWCS, higher DIN and lower TP values (Table 1), generally alternating with functional groups Y and M during the onset of the stratification period in summer (rainy period, Fig. 4B). After the disturbance events and the C. furcoides establishment, the biomass of blue-greens did not exceed 69.5 mm3 l-1 (June 2014). Biomass of C. furcoides was high in June and July 2015 (213.1 and 102.7 mm3 l-1, respectively). The same trends of total biomass and functionalgroup contributions were observed when comparing the surface and bottom water layers of Garc¸as Reservoir in 2017, except for June, when the total biomass (43.0 mm3 l-1) at the bottom exceeded that at the surface (27.7 mm3 l-1). Interestingly, at the bottom, the higher contribution of Ceratium furcoides was already apparent in March, 2 months earlier than the higher contributions seen at the surface (Fig. 5).

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Structural equation models A conceptual model showing the predicted relationships among the disturbances, the physical and chemical variables, and the species was constructed for testing (Fig. 6). The best-supported model included water transparency and SRP, as alternative variables for the factors physical and nutrients, respectively (Table 2; Fig. 7). The weight of evidence for this model, compared to the other candidate models, was rather strong for the data available (w = 0.80). The other models were poorly supported, although all the models fitted our data according to Fisher’s C statistic (P [ 0.05) (Table 2). The best model indicated that phytoplankton species and their interactions were affected by the disturbances of drought and water-hyacinth removal via changes in water transparency and SRP (Fig. 2). Specifically, changes in water transparency mediated by macrophyte removal decreased the abundance of Cylindrospermopsis (IE = - 0.24) and Microcystis (IE = - 0.19) and increased the abundance of Ceratium (IE = 0.17). Consequently, Cylindrospermopsis was negatively correlated with Microcystis (stdb = - 0.28) and Ceratium was positively correlated with Trachelomonas (std-b = 0.71). Furthermore, both water-hyacinth removal and drought were positively and indirectly related to Cryptomonas abundance via SRP concentration increase (IE = 0.32, and IE = 0.17, respectively). Two other direct effects on Fig. 6 Conceptual model showing the a priori predicted theoretical relationships among the disturbance (drought and macrophyte [water hyacinth] removal), physical (water transparency) and nutrient (SRP) factors, as well as biological (phytoplankton species) variables, for Garc¸as Reservoir. DIN dissolved inorganic nitrogen, TN:TP total nitrogen: total phosphorus, RWCS relative water-column stability, SRP soluble reactive phosphorus

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phytoplankton were detected: a negative relationship between water-hyacinth removal and Cylindrospermopsis (std-b = - 0.29); and a positive relationship between drought and Cryptomonas (std-b = 0.29) (Fig. 7).

Discussion The results demonstrated that the disturbance events played an important role in the phytoplankton changes, by modifying the abiotic conditions, disrupting the cyanobacterial steady-state periods in Garc¸as Reservoir (Bicudo et al., 2007) and opening a ‘‘window of opportunity’’ for C. furcoides. The management of the macrophyte bank (in July 2014) disturbed the sediment, causing significant increases in SRP and DIN concentrations, and probably fostered the activation of dormant propagules of Ceratium. At the same time, the historical drought (from June to August 2014) caused decreased the inflow from the city-zoo tributary, followed by an interruption during a period of 1–2 months, decreasing TP and chlorophyll a concentrations and leading to high water transparency. These environmental changes were sufficient to break the dominance of SN (Cylindrospermopsis raciborskii), since this species is sensitive to high light intensities (Reynolds, 1997). In turn, these changes likely allowed the recruitment of opportunistic mixotrophic species of functional group Y

Hydrobiologia Table 2 Information-theory results for six candidate models evaluating the relationships among key phytoplankton taxa and environmental drivers in the Garc¸as Lake. The expected relationships among taxa are depicted in Fig. 6. Physical drivers were represented, in alternative models, by water transparency (Secchi) and Relative Water-Column Stability (RWCS). Nutrients were represented by Soluble Reactive Phosphorus (SRP), total nitrogen and total phosphorus ratio

(TN:TP), and Dissolved Inorganic Nitrogen (DIN). Disturbances included drought and water hyacinth removal (whr). The column P-value is associated with the Fisher’s C statistic (Lefcheck, 2016). A P-value larger than 0.05 indicates that an a priori model fits the observed data. df Degrees of freedom, AICc akaike information criterion, delta AICc difference between the AICc of the i-th model and the AICc of the best model, w akaike weight delta AICc

w

Model

Biological

Disturbance 1

Disturbance 2

Nutrients

Physical

P value

df

AICc

Model 2

See Fig. 6

Drought

whr

SRP

Secchi

0.823

24

194.85

0.00

0.80

Model 3

See Fig. 6

Drought

whr

TN:TP

Secchi

0.634

24

198.35

3.50

0.14

Model 1

See Fig. 6

Drought

whr

DIN

Secchi

0.514

24

200.36

5.51

0.05

Model 5

See Fig. 6

Drought

whr

SRP

RWCS

0.212

24

206.49

11.64

0.00

Model 4

See Fig. 6

Drought

whr

DIN

RWCS

0.209

24

206.56

11.71

0.00

Model 6

See Fig. 6

Drought

whr

TN:TP

RWCS

0.187

24

207.21

12.36

0.00

Fig. 7 Best model fitted with piecewiseSEM (structural equation modeling) describing the relationships among disturbance (drought and macrophyte [water hyacinth] removal), physical (water transparency) and nutrient (soluble reactive phosphorus, SRP) factors, as well as biological (phytoplankton species) variables. Arrows indicate unidirectional effects. Solid lines represent significant relationships (P \ 0.05), and dashed lines

are non-significant relationships (P C 0.05). Black and red lines indicate positive and negative relationships, respectively. Values over the arrows denote the standardized effect size (regression coefficient, std-b) of each relationship. Line thickness is proportional to the effect size. R2 inside each box shows total marginal R2 considering only fixed-effect variables. Model selection is shown in Table 2

(Cryptomonas spp.). In addition, only small differences in temperature between the water-column layers were observed, due to the high water transparency, decreasing RWCS in the warmer periods and impeding the development of functional group M

(Microcystis), which is more likely to occur in stratified periods (Reynolds et al., 2002). Changes in resource availability, due to a pulse in resource supply, a decline in uptake by organisms, or both, may increase the susceptibility of a community to invasion (Davis et al., 2000). The disturbances in

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Hydrobiologia

Garc¸as Reservoir appear to have caused significant changes in resource availability, as shown by the best SEM model, which indicated that the increased SRP concentrations and water transparency were decisive for the changes seen in the phytoplankton. At the same time, the uptake of resources by SN and M organisms was probably prevented by either more light availability after macrophyte removal or lower RWCS, respectively. In addition to environmental changes, propagules of the organisms that will be recruited must be available in order for an invasion to occur (Padisa´k et al., 2010). Here, it is important to consider the propagules of Ceratium in the sediment. Indeed, several studies have indicated that the recruitment of Ceratium from cysts deposited in the sediment is determinant for the growth of planktonic populations (e.g., Reynolds, 1996; Rengefors et al., 2004). In Garc¸as Reservoir, Ceratium dominance at the surface was preceded by its high biomass at the bottom, strongly indicating that the sediment disturbance after macrophyte removal caused its recruitment in September 2014. Considering that the first occurrence of C. furcoides in two nearby reservoirs in the municipality of Sa˜o Paulo dates from 2008 (Billings and Guarapiranga reservoirs; Matsumura-Tundisi et al., 2010; Nishimura et al., 2015), one may wonder if it arrived in Garc¸as Reservoir earlier than its observed development in 2014. Assuming that this is plausible, then it might be possible that the recurrent cyanobacterial steady-state prevented Ceratium from invading before that. In addition to the encystment strategy, the morphology of Ceratium confers the ability to migrate vertically, low self-shading, potential low specific phosphorus requirements, ability for ‘‘luxury consumption’’ of phosphorus, and low rates of cell sinking and grazing (Pollingher, 1988). Some studies have shown that Ceratium may not necessarily be enhanced by nutrient abundance (Padisa´k, 1985). Thus, as seen in Garc¸as Reservoir, physical processes (increase in water transparency and decrease of RWCS) may be rather decisive in its establishment. Naselli-Flores & Barone (2003) recorded the highest development of functional group LM (Microcystis and Ceratium) in the period of high water transparency and before the onset of thermal stratification in a hypertrophic reservoir (Lake Arancio). Similarly, Matsumura-Tunidisi et al. (2010) related the effect of cold fronts on the water-

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column mixing to blooms of Ceratium furcoides in a Brazilian reservoir (Billings Reservoir). Studies have related extreme abiotic events, including anomalous drought periods, to phytoplankton dynamics (Naselli-Flores & Barone, 2003) and changes in biotic interactions (Kasprzak et al., 2017). In Garc¸as Reservoir, after the establishment of Ceratium, the following pattern emerged: low biomass of functional group M, co-occurring with Y, under low RWCS and low DIN; alternating with water-column mixing periods when SN was replaced by Ceratium in conditions of high availability of DIN, always coexisting with W2 (Trachelomonas spp.). This latter interaction was supported by the model, which showed a positive and significant relationship between Ceratium and Trachelomonas. Similarly to Ceratium, species of the genus Trachelomonas are bottom-dwelling organisms (Reynolds et al., 2002) and they are often found in the hypolimnia of transparent lakes (Reynolds, 1984; Becker et al., 2009). Therefore, the association between Trachelomonas and Ceratium may result from similar responses to an increase in water transparency. As no information on this relationship has appeared in the literature, little ecological information on euglenoids is available, and considering the lack of reports on Ceratium interactions with other phytoplankton species, the nature of the association between Trachelomonas and Ceratium abundance (similar responses to environmental changes or a biotic interaction) remains to be explored. The expected co-occurrence of Microcystis and Ceratium, commonly reported for temperate lakes, was not observed in Garc¸as Reservoir, where these species did not show a significant relationship. This suggests that the environmental modifications were, at first, more important in the recruitment of Ceratium than was competition with Microcystis. Although both species belong to the same functional group (LM) and share some functional traits (e.g., migration ability), Ceratium has been reported to have a much lower P content than Microcystis (Krivtsov et al., 2005). Since Ceratium is not occurring with Microcystis in the Garc¸as ecosystem, Ceratium should be assigned to the LO functional group (Reynolds et al., 2002; Padisa´k et al., 2009). However, considering the environmental context in which Ceratium was recruited and the blooming behavior in Garc¸as Reservoir, which shows many resemblances to the blue-

Hydrobiologia

greens including dominance over other species, Ceratium seems to belong more to LM than to LO. Another study has also classified C. furcoides as LM, even though it was not co-occurring with Microcystis (Naselli-Flores & Barone, 2003). Of the studies documenting Ceratium invasion in South America, only a few have mentioned other species found along with Ceratium (e.g., Matsumura-Tundisi et al., 2010; Nishimura et al., 2015). More studies and monitoring of the behavior of Ceratium will provide valuable information to identify occurrence patterns and/or new ecotypes in regions where this organism is invasive. Dominant algae may play major roles in structuring aquatic communities and ecosystem characteristics (Padisa´k et al., 2010). This pattern seems to occur in Garc¸as Reservoir, as alternative states between Ceratium-W2 and M-Y have repeated since Ceratium became established (3 consecutive years), and Ceratium blooms increase light penetration, sustaining the interactions resulting from these physical changes and fostering the dominance of flagellated phytoplankters. Recently, Meichtry de Zaburlı´n et al. (2016), exploring the potential distribution of Ceratium furcoides in South America, determined that the areas most susceptible to its invasion were mainly concentrated in the basins from southeastern Brazil to northeastern Argentina, especially due to temperature. The authors warned of the possibility of increased blooms because of climate change. Considering the disturbances related to climate and its effects on physical forces in lakes and reservoirs, structural and dynamic changes in phytoplankton communities can be expected (Winder & Hunter, 2008). In general, disturbances tend to favor invasions, and stressed ecosystems may be especially susceptible (Strayer, 2010). Accordingly, the interactions identified in Garc¸as Reservoir suggest that the establishment of Ceratium, after benefiting from the disturbance events (drought and water-hyacinth removal), modified the environmental conditions, such as the relatively lower water-column stability due to the high transparency and consequently the phytoplankton dynamics and interspecific interactions. Since then, flagellated forms became dominant in Garc¸as Reservoir and alternative states between Ceratium-W2 and M-Y have been repeated. In other words, Cyanobacterial dominance now tends not be the rule in this tropical reservoir, as the skillful Ceratium apparently has come to stay. Time will tell.

Acknowledgements The authors are indebted to FAPESP, Fundac¸a˜o de Amparo a` Pesquisa do Estado de Sa˜o Paulo and to CNPq, Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico for providing several funds and grants over these years. DCB and CEMB thank CNPq (Conselho Nacional de Desenvolvimento Cientı´fico) for Research Fellowships (310404/2016-9 and 303876/2004-2). We are profoundly grateful for the valuable support of undergraduate and graduate students, as well as the technicians for their continuous support in the field and the laboratory over these many years. We also thank Yukio Hayashi da Silva for improving the illustration of the study area.

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