Fish functional diversity responses following flood

Accepted: 1 March 2018 DOI: 10.1111/eff.12402

ORIGINAL ARTICLE

Fish functional diversity responses following flood pulses in the upper Paraná River floodplain Matheus T. Baumgartner1

 | Anielly G. de Oliveira1 | Angelo A. Agostinho1,2,3 | 

Luiz C. Gomes1,2,3 1

Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais (PEA), Universidade Estadual de Maringá (UEM), Maringá, PR, Brazil

2

Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupélia), Maringá, PR, Brazil 3

Departamento de Biologia (DBI), Centro de Ciências Biológicas (CCB), Universidade Estadual de Maringá (UEM), Maringá, PR, Brazil Correspondence Matheus T. Baumgartner, Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais (PEA), Universidade Estadual de Maringá (UEM), Maringá, PR, Brazil. Email: [email protected]

Abstract Flood pulses are the main force driving the dynamics of aquatic communities in floodplains. The responses of communities to environmental changes following flood pulses usually demand a time lag to appear and reach the climax. We assembled a data set of 16 years of fish samplings to assess the relationship between water level and four functional diversity measures, in the upper Paraná River floodplain. Specifically, we approached four aspects of each relationship between water level and functional diversity: nature (positive or negative), sensitivity (response intensity), responsiveness (response delay) and extent (response duration). The nature of the relationship between water level and functional diversity was positive in all cases. Functional richness (FRic) responded right after flood pulses, although with shorter extent. Abundance-­dependent functional measures (evenness—FEve; divergence— FDiv; and Rao’s quadratic entropy—Rao’s Q) presented delayed responses, reaching peaks more than 1.5 years after flood pulses. Significant effects of floods on fish functional diversity were observed for more than 3 years, although the highest functional diversity was observed with 1.8 years, on average. More importantly, flood pulses had no longer significant effects on functional diversity after 4 years. Regarding conservation strategies in regulated systems, flood events should occur every 2 or 3 years, with adequate timing (October-­ November), intensity (up to 450 cm) and duration (at least 50 uninterrupted days). Intervals longer than 3 years or inadequate timing, intensity and duration could dramatically decrease functional diversity and compromise ecosystem services. KEYWORDS

cross-correlation function, disturbance, fish assemblage, flood legacy, functional ecology, time lag

1 |  I NTRO D U C TI O N

1989; Poff et al., 1997), but anthropogenic interventions have severely affected this dynamics (Agostinho, Gomes, & Pelicice, 2007;

In aquatic systems, environmental alterations caused by variations

Agostinho, Gomes, Santos, Ortega, & Pelicice, 2016). The intensity

in natural river flow regimes change ecosystems structure and func-

and timing of flood pulses are determined by the amount of precipi-

tioning (Bunn & Arthington, 2002). Especially in river–floodplain sys-

tation in the whole watershed, which is in turn subjected to climatic

tems, the annual increase in water level, known as the flood pulse,

variations. As a result, there will be a wide sequence of events, which

is the main force driving these changes (Junk, Bayley, & Sparks,

influence biological communities differently from year to year (Junk

Ecol Freshw Fish. 2018;1–10.

wileyonlinelibrary.com/journal/eff   © 2018 John Wiley & Sons A/S. |  1 Published by John Wiley & Sons Ltd

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BAUMGARTNER et al.

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et al., 1989; Pinaya et al., 2016). The flood pulse modifies limno-

the flood and enhanced population recruitment (Bice et al., 2014;

logic conditions and community structures (Thomaz, Pagioro, Bini,

Junk et al., 1989; Pereira, Tencatt, Dias, Oliveira, & Agostinho, 2017;

Roberto, & Rocha, 2004). Therefore, species that take advantages of

Ward & Stanford, 1995).

the flood/drought dynamics, through adjustments of their life strat-

Thus, the objective of this study was to evaluate the effects

egies, are selected along the evolutionary process (Junk et al., 1989;

of flood pulses on fish functional diversity in the upper Paraná

Neiff, 1990). Thus, aquatic species are very dependent on natural

River floodplain, a free remnant stretch downstream of a series of

hydrological regimes, especially fish.

dams. Functional diversity (FD) was assessed from four measures

The construction and operation of dams dramatically affect

(Functional Richness–FRic; Functional Evenness—FEve; Functional

the dynamic of fish populations downstream through alterations in

Divergence—FDiv; and Rao’s quadratic entropy—Rao’s Q), and each

the flood regime (Agostinho, Thomaz, & Gomes, 2004; Agostinho

one was separately correlated with water level. The use of four com-

et al., 2007, 2016). Impoundments redistribute the river discharge

plementary functional measures provides a more embracive view of

in space and time, increasing minimum and decreasing maximum

the effects of floods on fish fauna because each diversity measure

flows, changing the dynamic and functioning of downstream eco-

has a particular potential to reveal community-­structuring processes

systems (Agostinho, Pelicice, & Gomes, 2008; Petts, 1984). The

(Mouchet, Villéger, Mason, & Mouillot, 2010). Precisely, we intended

most affected process is the connectivity among microhabitats,

to provide numeric-­based answers for four questions: (i) Does the

which tends to influence the dynamics of species (Agostinho,

flood pulse have a positive relationship with different measures

Pelicice, et al., 2008; Bailly, Cassemiro, Winemiller, Diniz-­ Filho,

of fish functional diversity? (ii) Which measure has the fastest re-

& Agostinho, 2016; Gubiani, Gomes, Agostinho, & Okada, 2007),

sponse? (iii) Which response reaches its fullness (climax) first? (iv)

including the functional diversity (Oliveira, Baumgartner, Gomes,

Which is the long-­lasting response?

Dias, & Agostinho, 2018; Röpke et al., 2017; White, Ondračková, & Reichard, 2012).

We predicted that the relationship between water level and functional diversity would be positive. Functional diversity mea-

Responses of communities to changes in environmental condi-

sures that consider only the diversity of traits (FRic) would have a

tions usually appear after some elapsed time (relaxation times) (Essl

faster (in time) and shorter (in duration) response, while measures

et al., 2015a,b). Due to these delayed responses to disturbance as

related to species abundance and evenness (FEve, FDiv, and Rao’s Q)

floods (or their absence, as in extended droughts), it is necessary

are expected to present delayed but more intense and long-­lasting

to evaluate the structure and composition of fish assemblages over

responses. To answer these four questions, we assessed four char-

time, so that reproduction and recruitment can be effective and

acteristics of the relationship between water level and each of the

reflect these disturbances. In addition, an extended temporal per-

functional diversity measures: nature (positive or negative); sensi-

spective is important because it includes alternation between flood

tivity (i.e. intensity; relative height of the perceived response peak);

and dry years. As floods increase dispersion of individuals and colo-

responsiveness (i.e. delay; time-­lag of the perceived response); and

nisation of microhabitats (Junk et al., 1989; Thomaz, Bini, & Bozelli,

extent (i.e. duration of the response) through analyses of 16 years of

2007), droughts increase the spatial heterogeneity, once each mi-

continuous data. We employed a technique that considers a variety

crohabitat can follow its own ecological succession after isolation

of facets of the cause–effect relationship (cross-­correlation function

(Thomaz et al., 2007). Prolonged droughts usually reduce local spe-

analysis and its prewhitened extension), and our results may provide

cies richness and abundances via resources limitation and compet-

valuable information for the management of fish diversity in dam-­

itive exclusion, even leading to local extinctions (Hitt & Chambers,

regulated floodplains.

2014; Medeiros & Arthington, 2014; Petry, Agostinho, & Gomes, 2003). Nevertheless, traditional taxonomic diversity measures cannot detect subtle changes until an advanced stage of modification is reached (Miranda et al., 2005). Thereby, the functional approach,

2 | M E TH O DS 2.1 | Study area

which considers the ecological roles of species instead of their tax-

The upper Paraná River basin is the most important arrangement of

onomic identity, seems to be more sensitive to discrete changes in

rivers in Midwest and Southern Brazil, and also the most impounded

community features. Functional diversity embraces the composition

basin in South America. The surveyed floodplain is situated between

of species traits and life-­history strategies and also reveals more

Porto Primavera Dam (North) and Itaipu Reservoir (South) and is the

about the ecosystem responses to environmental changes (Kearney

last remaining free-­flowing stretch of this river (230 km long) inside

& Porter, 2009; Petchey & Gaston, 2006). This approach apparently

Brazil (Figure 1). This floodplain is located at the west margin of the

offers advantages over taxonomic or single-­trait analyses because

river, composed by different biotopes (microhabitats) as floodplain

natural selection operates on many interacting traits simultaneously

lakes, channels and rivers with distinct degrees of connectivity. This

(Hitt & Chambers, 2014). Based on the premise that flood pulses in-

river stretch is regulated by the cascade of dams upstream, but re-

crease diversity and abundances of communities, it is expected that

ceives large tributaries and still has marked water level variations,

fish functional diversity increase after certain time following a flood

although not as intense and frequent as before dams were built

event. This is due to the greater resources availability provided by

(Gubiani et al., 2007).

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BAUMGARTNER et al.

F I G U R E   1   Location of the sampling sites in the upper Paraná River floodplain (1—main channel; 2—permanently connected lake; 3—temporarily connected lake)

The fish fauna of the upper Paraná River is composed of more

(registration number 64575000). The time-­series for this variable

than 180 species (Graça & Pavanelli, 2007), but it is believed that this

was composed by the arithmetic mean of daily WL for the entire

number could surpass 200 species, after taxonomic review (unpub-

months when fish were collected.

lished data). Particularly, in the floodplain, species with a variety of

The average water discharge for this stretch of the Paraná River

life strategies occur, from large-­bodied migratory species to seden-

is slightly over 9,000 m³/s, at the water level of 350 cm (Souza Filho,

tary and small ones (Agostinho et al., 2004).

2009). A threshold of 450 cm was previously established as the water level at which the Paraná River floods the plain (Comunello,

2.2 | Sampling

Souza Filho, Rocha, & Nanni, 2003). At this level, the average river discharge exceeds 12,300 m³/s and floods 29% of the 359 km² of

Sampling was conducted quarterly from February 2000 to November

the floodplain (Oliveira, Suzuki, Gomes, & Agostinho, 2015; Rocha,

2015 in three sampling sites: (1) the main channel of the Paraná

Santos, & Souza Filho, 2001).

River, (2) one lake continuously connected to the Paraná River and (3) one lake disconnected from the Paraná River during low waters. These three sites were chosen because they cover all the spatial heterogeneity and were continuously sampled in this period. Fish were

2.3 | Functional traits and functional diversity measures

caught with standardised effort using gillnets with different mesh

Functional traits were selected based on the ecological role of each

sizes (4, 5, 6, 7, 8, 10, 12, 14 and 16 cm between opposite knots), set

species and the relationship with ecosystem processes. They were:

for 24 hr at each sampling site. Captured fish were anaesthetised

feeding (detritivores, invertivores, insectivores, piscivorous, omni-

with 5% benzocaine, sacrificed, identified to species, counted and

vores, herbivores or planktivores); habitat use (demersal, benthope-

measured the standard length. To better evaluate the effect of water

lagic or pelagic); long-­distance migratory (>100 km) or nonmigratory;

level on functional diversity, we polled the samples of the three loca-

parental care and internal fertilisation or their opposite; mouth posi-

tions according to months. We performed this because the sampling

tion (lower, subterminal, terminal or superior); and maximum total

sites are located less than 8 km apart, and they belong to the same

length. Except for the last trait, estimated from collected data, the

waterscape during high water levels. Although this procedure elimi-

others were obtained from the literature (Data S1). The use of mul-

nates among-­site variation, pooling samples are justified because

tiple traits produces a Hutchinson’s niche with various dimensions,

our main focus was on the long-­term temporal trends related to

which better defines the functional units than the use of few traits,

water level variations, rather on the spatial variations.

as feeding and habitat only (Wilson, 1999).

Hydrologic data were provided by the National Water Agency

The chosen functional diversity (FD) measures were: richness,

(Agência Nacional das Águas—ANA; Sistema Nacional de Informações

evenness, divergence (Villéger, Mason, & Mouillot, 2008) and Rao’s

Sobre Recursos Hídricos—SNIRH) obtained through daily water level

quadratic entropy (Rao′s Q; Botta-­Dukát, 2005). Functional richness

(WL; cm in relation to the operation of the Hydrometric Station at

(FRic) represents the diversity of combination of traits (species) in a

231.8 m a.s.l.) measures at the Porto São José Hydrometric Station

community, measured as the hypervolume occupied in a functional

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BAUMGARTNER et al.

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F I G U R E   2   Summary of the analytical protocol used to evaluate the characteristics of the relationship between water level (WL) and each functional diversity measure (functional richness (FRic); functional evenness (FEve); functional divergence (FDiv); and Rao’s quadratic entropy (Rao’s Q)), in the upper Paraná River floodplain. Ordinary cross-­correlation functions (CCF) were used to assess the nature (N) and the extent (E), while prewhitened cross-­ correlation functions (pw-­CCF) were used to assess the sensitivity (S) and the responsiveness (R) of the relationship space by all species in a community. Functional evenness (FEve)

cross-­correlation function (CCF) analysis (Chatfield, 1996; Probst,

addresses how similar are the abundances of the species within a

Stelzenmüller, & Fock, 2012). CCF performs time-­lagged correlations

community, measured as the regularity of abundance distributions

between an influential time series, representing a disturbance or an

of all species in the functional space. Functional divergence (FDiv)

environmental change (i. e. WL) and the affected time-­series, which

quantifies the representativeness of the abundances of the more un-

represents a variable expected to exhibit a delayed response (i. e.

common combinations of traits, measured as the proportion of total

FD measures). To explore the response of each FD measure to flood

abundance supported by the species with the most extreme trait val-

events, two types of CCFs were applied between WL and each FD

ues (near the border of the functional space). While Rao’s Q reflects

measure: ordinary CCF and prewhitened CCF. Due to our sampling

both the distribution of abundances and the dissimilarities among

design, each lag in all time-­series corresponded to the elapsed time

traits combinations, quantified as the relationship between relative

of 3 months.

abundances and the species pairwise distances (Botta-­Dukát, 2005;

Ordinary CCF performs simple time-­lagged correlations be-

Mouillot, Graham, Villéger, Mason, & Bellwood, 2013). All mea-

tween two time-­s eries and was used to assess the nature of the re-

sures were calculated using the function “dbFD” (Distance-­Based

lationship and the extent of the effects of WL on FD. The nature of

Functional Diversity) from package “FD” (Laliberté & Legendre,

the relationship (nature of the correlation, positive or negative; N

2010) in R Environment (R Core Team, 2016), using Gower dissim-

in Figure 2) represents whether the higher values of the influential

ilarity with Cailliez’s correction for negative eigenvalues (Legendre

time-­s eries produce higher values in the affected time-­s eries. The

& Legendre, 1998).

extent (lag at which there are no longer significant correlations; E in Figure 2) indicates for how long the effects remain in the re-

2.4 | Data analysis

sponse variables. Prewhitened CCF (pw-­CCF) works similar to ordinary CCF, with the advantage of removing spurious correlations

The time series of all variables were previously transformed to stabi-

from the affected time-­s eries, based on temporal autocorrelations

lise variances (log: WL, FDiv, Rao’s Q; squared: FRic, FEve) (Shumway

in the influential time-­s eries. This is done by fitting an autoregres-

& Stoffer, 2011) and then used in this form for the following steps.

sive integrated moving average (ARIMA) model and turning the

Stationarity was assessed using the slope coefficient of a linear

affected time-­s eries into “white noise” (Box & Jenkins, 1976). This

model, and nonstationary series were first-­differenced to meet this

second type of CCF was needed to assess the sensitivity (strength

assumption. A summary of the analyses and interpretation is pro-

of the pw-­CCF peak; S in Figure 2), representing the intensity of

vided in Figure 2.

the response, and the responsiveness (lag of the pw-­CCF peak; R

The nature of the relationship between a disturbance and its response and how they are correlated in time can be observed through

in Figure 2), representing the delay of the response (as suggested by Probst et al., 2012).

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BAUMGARTNER et al.

In the graphical results of the CCFs, upward bars represent positive relationships, while downward bars represent negative relationships and the height of each bar represents the strength of the relationship. As a default of the method, although with negative values, the left quadrants of the graphics represent positive time lags, when the change in the affected (i. e. functional diversity measures) time-­series occurs chronologically after the change in the influential (i. e. water level) time-­series. In opposite, the right quadrants represent negative time lags (for details, see Probst et al., 2012). In our case, assuming that the influence of any FD measure on WL is ecologically meaningless, only the left quadrants of the CCFs are of interest. Significant CCFs in the upper left quadrant indicates positive relationship between variables, while significant CCFs in the lower left quadrant indicates negative relationships. The significance of CCFs and pw-­CCFs is achieved using Bartlett’s critical values (α = .05) at ±2/√n, where n is the length of the time-­series (Berryman & Turchin, 2001). CCFs and pw-­CCFs were performed using functions “ccf” from package “stats” and “prewhiten” from package “TSA” respectively (Chan & Ripley, 2012), in R Environment (R Core Team, 2016). The R routines, short descriptions and partial data on water level and FRic are available in Data S2 to ensure the reproducibility of the analysis.

3 | R E S U LT S All captured fish belonged to 113 species from orders Characiformes, Siluriformes,

Cichliformes,

Gymnotiformes,

Myliobatiformes,

Pleuronectiformes and Synbranchiformes. Along the 16 years of this study, the time-­s eries for WL presented four flood pulses with amplitudes of at least 200 cm (2002 and 2006), two of them with increases greater than 250 cm (2010 and 2011), reaching water levels near 600 cm, flooding the entire plain (Figure 3a). These floods were caused by intense rains, especially in the north and east portions of the Paraná River basin, and always occurred in the summer (rainy season), between November and March. All FD measures presented high variability without clear trends (Figures 3b, c, d, e). All time-­s eries met the stationarity assumption, except for Rao’s Q that required first differentiation. The ordinary CCFs showed that the nature of the relationships between WL and all FD measures were positive and significant in all cases (Figure 4), although the extent of the effects varied. The shortest extent was observed for FRic (Figure 4a), for which the

F I G U R E   3   Time-­series of (a) water level (WL); (b) functional richness (FRic); (c) functional evenness (FEve); (d) functional divergence (FDiv); and (e) Rao’s quadratic entropy (Rao’s Q). Each time lag corresponds to the elapsed time of 3 months. All time-­ series are expressed in original values, without any transformation, but for the analysis, all variables were transformed to stabilise variances (log: WL, FDiv, Rao’s Q; squared: FRic, FEve), and Rao’s Q was first-­differenced to meet the stationarity assumption

effects were no longer observed after lag-­5. In opposite, the extent of the effects was long-­s tanding for the other FD measures, from lag-­12 for FDiv (Figure 4c), lag-­14 for Rao’s Q (Figure 4d), until

revealed that the time elapsed, from the disturbance until their par-

lag-­15 for FEve (Figure 4b), when no more significant effects were

ticular effects reached fullness (climax), was considerably different

observed.

for each measure. FRic was more responsive, at lag-­4 (Figure 5d),

Considering the prewhitened CCFs, the sensitivity approach evi-

compared to Rao’s Q and FEve, at lag-­7 and lag-­11 respectively,

denced that the strength of the disturbances effects differed among

(Figures 5e and 5b). Finally, FDiv presented the most delayed re-

the FD measures, decreasing in the order FRic, Rao’s Q, FEve and

sponsiveness, at lag-­23, but with a noticeable value at lag-­7, although

FDiv (Figure 5). Most importantly, the responsiveness approach

not significant (Figure 5c).

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BAUMGARTNER et al.

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F I G U R E   4   Ordinary cross-­correlation functions (CCFs) between water level (WL) and each FD measure (a) functional richness (FRic); (b) functional evenness (FEve); (c) functional divergence (FDiv); and (d) Rao’s quadratic entropy (Rao’s Q). Dashed lines indicate the significance threshold (α = .05)

4 |  D I S CU S S I O N

F I G U R E   5   Prewhitened cross-­correlation functions (pw-­CCFs) between water level (WL) and each FD measure (a) functional richness (FRic); (b) functional evenness (FEve); (c) functional divergence (FDiv); and (d) Rao’s quadratic entropy (Rao’s Q). Dashed lines indicate the significance threshold (α = .05)

the species throughout the entire floodplain, due to the connectivity of the mosaic; (ii) increase in food and shelter availability, as a

All measures of fish functional diversity were positively related to

consequence of flooding vegetated areas; and (iii) successful repro-

water level. Although this is not a novelty, these results reinforce the

duction of most fish species, especially migratory, triggered and syn-

flood pulse as a main driver of fish assemblage structure. However,

chronised by the water level rising and the flood peak (Agostinho,

we did not observe positive effects of water level after 3 years, sug-

Bonecker, & Gomes, 2009; Agostinho et al., 2004; Fernandes et al.,

gesting that flood events should not have intervals longer than this.

2009; Vazzoler, 1996). In fact, all reproductive strategies, except

The functional diversity measure that had the fastest response and

short-­distance migratory, are particularly dependent on the occur-

first reached the climax was related to the variety of traits (i.e. func-

rence of floods to perform longitudinal migrations (Bailly, Agostinho,

tional richness—FRic), while measures related to the distribution of

& Suzuki, 2008). Although affecting all reproductive strategies

abundances (i.e. functional evenness—FEve, divergence—FDiv, and

(Agostinho et al., 2004), migratory species were those that bene-

Rao’s Q) took almost 2 years to reach their fullness. More impor-

fited the most from flood events. These species depend on an or-

tantly, our results reveal that the increase in functional diversity

dered sequence of events to perform migrations, which increases

caused by a flood pulse is, on average, no longer observed after

the recruitment of individuals and allow young individuals to access

4 years.

nursery areas (Gubiani et al., 2007).

The positive effects, evidenced by the increase in all measures

Each flood pulse event has its own peculiarities of timing, inten-

of functional diversity following the flood pulse events, may be re-

sity and duration, from year to year, affecting biotic communities

lated to three main aspects: (i) dispersion of individuals of most of

differently (Pereira et al., 2017). The recruitment success and the

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BAUMGARTNER et al.

persistence of fish populations are straightly dependent on timing

The functional diversity measures that consider species abun-

and duration of floods (Agostinho, Gomes, Veríssimo, & Okada,

dances responded later but also showed strong effects of flood

2005; Gomes & Agostinho, 1997; Gubiani et al., 2007; Oliveira et al.,

events. Functional divergence and Rao’s Q reached the response

2015). In addition, greater flood events also increase the survival

peak almost 2 years after the flood event, while functional even-

rates of larvae and young of most species (Agostinho et al., 2004;

ness took almost three. This delayed response was expected for

Lowe-­McConnell, 1987; Machado-­Allison, 1990).

abundance-­based measures because it requires the succession of

The flood pulse also influences species abundance by affecting

reproductive cycles to enhance cohorts and increase abundances.

different feeding strategies. The submerging of a great amount of

Controversially, the positive response of the functional divergence

vegetation increases the availability of food, especially for herbiv-

reveals an increase in the abundance of species with a more singular

orous species. In years of pronounced floods, Abujanra, Agostinho,

combination of traits, which are usually imperilled by disturbances

and Hahn (2009) observed a positive relationship between herbiv-

(Mouillot et al., 2013). These species are more specialised compared

orous body condition and the coefficient of variation of the annual

to others with more common traits and are located in the centre of

water level of the Paraná River, demonstrating that these fluctua-

the functional space. In our study, these specialised species were mi-

tions led to gain in weight for this group. In addition, species that

gratory and large-­bodied, corroborating the positive effect of flood

could turn leaves and other plant parts into their main food source

events on their abundances, which required a longer time to appear

also have a potential to benefit from phases of flooded vegetation.

because the initial life stages of these species takes more time to

For the other strategies, however, these same authors found that

develop.

the body condition of the species was higher in drought years than

Therefore, the completion of hydrologic cycles, involving con-

in years of pronounced floods. This was addressed to the fact that

nection and isolation of biotopes, is fundamental for all fish species,

drought phases provide resources with higher nutritional quality

from migratory (favored during high water periods) to feeding-­

than flood phases. Enhanced body conditions increase the probabil-

specialised species. This alternation between the phases of a hy-

ity that individuals will carry out reproductive migrations (Engelhard

drologic cycle allows migratory species to complete their life cycle

& Heino, 2006), increase fecundity, and the diameter and viability

and determines the increase in fitness and persistence of special-

of the eggs (Thorsen, Marshall, & Kjesbu, 2006), positively affecting

ised species, which are better competitors in isolation conditions

fitness. Thus, in addition to the importance of floods, the previous

(Abujanra et al., 2009). Complementarily, the embracive aspect of

and subsequent low water periods are of equivalent importance for

the positive effects of flood events on the entire fish assemblage is

species and should not be overlooked. In this way, the availability of

revealed by the delayed increase in functional evenness, which de-

food resources for the ichthyofauna, as well as the nutritional value

pends that the proportional abundances of all species become more

and digestibility of food, are directly and indirectly dependent on

similar to show an increase.

flood pulse events and provide better conditions for fish through the following hydrologic phases.

Regarding the extent (or duration) of the effects of flood pulses on fish functional diversity, the pattern of the long-­lasting effects

Considering the different features of each functional diversity

was the opposite of the responsiveness. Reasonably, the effects that

measure, in terms of responsiveness and sensitivity, the functional

reached their fullness earlier had shorter durations. The significant

richness had the fastest response and presented the strongest ef-

effects of floods on abundance-­based functional measures were ob-

fect. This might be addressed to a discrete increase in taxonomic

served for almost 4 years after the flood events. More importantly,

richness in all microhabitats of the floodplain, due to the higher

no effect was observed after these 4 years for all functional diver-

dispersion of individuals during high water phases (Agostinho &

sity measures, which means that the effects of a given flood event

Zalewski, 1995; Rodríguez & Lewis, 1994). Fish were confined

were no longer effective after this period.

during the drought, which accentuated interspecific interactions

Although the effects of flood events were observed for more

such as competition and predation, leading to local extinctions and

than 3 years, the highest functional diversity was observed within

reduction in local taxonomic diversity. Specifically, studies report a

1.8 years, on average. However, the simplest way to understand

direct relationship between taxonomic and functional richness for

the importance of a higher fish functional diversity is to focus on

fish (Carvalho & Tejerina-­Garro, 2015; Oliveira et al., 2018; Pool &

the opposite: what are the consequences involving decreases in fish

Olden, 2012). Therefore, functional richness will follow taxonomic

functional diversity. Lowering functional diversity is related to two

richness decrease. During flood pulses, biotic homogenisation oc-

main causes: loss of species, and consequently traits (e.g. local or

curs (Thomaz et al., 2007) and locally extinct species reappear in

regional extinction) and/or substantial decrease in their abundances

samplings, through dispersion during high waters, sourced from sites

(Mouillot et al., 2013; Villéger, Miranda, Hernández, & Mouillot,

in which they persisted. In a year, and almost instantaneous com-

2010). The concerns surrounding this decrease are well synthesised

pared to the other functional measures, the positive effects of flood

by Vitule et al. (2017). Functional diversity loss can affect species in-

pulses were observed for functional richness. As this measure con-

teractions and ecosystem processes (Correa et al., 2015; Pendleton,

siders the diversity of traits and the higher its value, the larger the

Hoeinghaus, Gomes, & Agostinho, 2014), which are the main binding

functional volume occupied without regard to density, it increased

mechanisms in aquatic environments. Particularly, overexploitation

during and right after the flooding period.

and the decrease in some populations may lead to loss of species

|

BAUMGARTNER et al.

8      

that modifies the environment (“ecosystem engineers”), which have an important role in nutrient dynamics, primary and secondary productivity and sustain assemblage structures (Flecker et al., 2010; Mormul, Thomaz, Agostinho, Bonecker, & Mazzeo, 2012; Taylor, Flecker, & Jr Hall, 2006). Usually ignored, rare species also have proven to be important for the maintenance of the functional structure of fish assemblages (Leitão et al., 2016). Along with the threat relating species loss and lowering functional diversity, the series of dams upstream from this floodplain controls the water discharge depending on energy demand, not on natural requirements anymore. There are strong pieces of evidence demonstrating that this regulation by dams affects the entire biotic structure of floodplains (Agostinho et al., 2004) and causes functional simplification of the fish assemblage in a long-­term (Oliveira et al., 2018). Some studies in impoundments reveal that seasonal manipulations of water level (Benejam, Benito, Ordóñez, Armengol, & García-­Berthou, 2008; Cooke, 2005; Paller, 1997) are successful and equivalent to restore elements of the natural flood pulse to a floodplain lake (Bayley, 1991). Besides, the applicability of the manipulation of the water level has been effective to increase biodiversity in this floodplain (Agostinho, Gomes, Pelicice, Souza-­Filho, & Tomanik, 2008; Luz-­A gostinho, Agostinho, Gomes, Júlio-­Júnior, & Fugi, 2009). Finally, following two main premises (i) the decrease in functional diversity affects ecosystem processes, and (ii) we found that flood pulses do have a particular potential to increase the fish functional diversity of the floodplain, we come to some conclusions. Regarding conservation management strategies, in the best case, it is of utmost importance that flood events should not have intervals longer than 3 years. The best setting for flood events, regarding periodicity, is to occur every 2 or 3 years, no longer. Specifically, the integrated operation of upstream dams should provide sufficient water to raise the Paraná River level up to 450 cm. The ideal timing of flood occurrence is in October and November, while the duration should be of at least 50 uninterrupted days (following Agostinho et al., 2004; Agostinho, Gomes,et al., 2008; Suzuki et al., 2009; Luz-­A gostinho et al., 2009; Oliveira et al., 2015).

AC K N OW L E D G E M E N T S We thank all Nupélia staff for years of field and laboratory work collecting and analysing this data. MTB and AGO thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the Ph.D. scholarship. AAA thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for productivity scholarship. We also thank two anonymous reviewers for their helpful comments.

ORCID Matheus T. Baumgartner  org/0000-0001-7472-8588

http://orcid.

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How to cite this article: Baumgartner MT, de Oliveira AG, Agostinho AA, Gomes LC. Fish functional diversity responses following flood pulses in the upper Paraná River floodplain. Ecol Freshw Fish. 2018;00:1–10. https://doi. org/10.1111/eff.12402