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Consequences of agroindustrial sugarcane production to freshwater biodiversity

May 2015
GCB Bioenergy 8(3)

DOI:10.1111/gcbb.12279

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Authors:

Luis Schiesari

University of São Paulo

Décio Tadeu Corrêa

University of Texas at Austin

The environmental benefits of a broad scale adoption of biofuels are critically contingent on what current land uses will be converted for feedstock expansion and how converted land will be managed. We assessed the consequences of land use and land management for the agroindustrial production of sugarcane to the physical, chemical and biological properties of freshwater systems. We surveyed 16 environmental variables and algae, tadpoles, predatory invertebrates and fish in lentic water bodies distributed across a gradient in land use intensity ranging from seasonal Atlantic Forest and cerrado to pastures to sugarcane plantations in SE Brazil, the most important sugarcane-producing region in the world. The gradient in land use intensity was not only an axis of native habitat loss but also of ecosystem productivity, as indicated by increased conductivity, turbidity, and phytoplankton biomass. Land use had a clear signal on community and metacommunity organization, with converted land being impoverished in biodiversity relative to native habitats. However, frequency of occurrence, density, biomass and alpha diversity of tadpoles and their predators were not affected by land use. These results suggest that sugarcane fields function as habitat to a fraction of aquatic biodiversity. Within sugarcane fields, larger wetlands surrounded by buffer strips as required by law appeared comparatively buffered against land management practices and housed a disproportional fraction of animal biomass, likely acting as sources of migrants to other water bodies in the landscape. Conversion of pastures to sugarcane fields, suggested as a strategy to reduce competition for land with food production and biodiversity conservation, does not appear to have strong consequences to lentic freshwater systems, provided that wetlands and surrounding buffer strips are preserved. These observations emphasize the importance of enforcement of legislation regulating land use (i.e. the ′Forest Code′) and certification systems rewarding the voluntary adoption of better land management practices.This article is protected by copyright. All rights reserved.

Effects of land use on selected environmental variables related to water body structure (left), water physicochemistry (middle) and productivity (right). See Table S1 for univariate statistical analyses. Data from both sampling surveys are lumped for each response variable. Because in each land-use water bodies were selected so as to cover the full spectrum of the hydroperiod gradient, the inclusion of area and hydroperiod in this figure is meant to demonstrate that this important gradient was controlled in our sampling surveys. Corrected α = 0.002.

…

MDS plots of the environmental (left) and tadpole community (right) data from water bodies distributed across a gradient in land-use intensity comprising native habitats, pastures, and sugarcane plantations. Black triangles = sugarcane plantations, gray squares = pasture, open circles = native habitats. Environment plot based on the Euclidian distance of 16 log-transformed environmental variables. Stress value = 0.153. Tadpoles plot based on the Bray–Curtis distance of 21 tadpole species Hellinger-transformed density data. Stress value = 0.082.

…

Frequency of occurrence (b) Density (c) Per-unit-area biomass (d) Richness per pond and (e) Richness per land-use type of tadpoles (left) and predators (right) in water bodies distributed across a gradient in land-use intensity comprising native habitats, pastures, and sugarcane plantations. Here frequency of occurrence refers to the % of water bodies that contained tadpoles or predators in either the first (December) or second (February) community surveys. Density and per-unit-area biomass boxplots lump data from both surveys, and richness per pond and richness per land-use type consider the cumulative species list found in a given pond (or land use) across surveys. Richness for amphibians is species richness, for invertebrates (which include dragonflies, water bugs, beetles, and fish) is family richness. Because few fish species were captured by pipe sampling, estimates of predator richness include fish captured by seine nets as well. Land use had a significant effect in (e) but not in (b), (c), or (d). See Table S1 for univariate statistical analyses.

…

Amphibian species-by-site incidence matrix for the Estação Ecológica do Jataí and surrounding agricultural areas. The matrix is ordered by reciprocal averaging such that water bodies with the most similar species lists and species with the most similar distributions are closest together. Position of each water body across three important freshwater environmental gradients is represented in color coded rows at increasing shades of gray at the top of each matrix (intensity of land use: native habitats, pastures and sugarcane plantations; hydroperiod: 0–49%, 50–99%, and 100% days with water; canopy cover: 0–33%, 34–66%, and 67–100% canopy cover). Arrows display environmental factors significantly associated with site ordination scores according to a Spearman rank correlation.

…

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Consequences of agroindustrial sugarcane production to

freshwater biodiversity

LUIS SCHIESARI

and D



ECIO T. CORR

Environmental Management, School of Arts, Sciences and Humanities, University of S~

ao Paulo, Av. Arlindo B

ettio 1000,

03828-000, S~

ao Paulo-SP, Brazil,

The University of Texas at Austin, Department of Integrative Biology, 1 University Station,

C0990, Austin, TX 78712, USA

Abstract

The environmental beneﬁts of a broad-scale adoption of biofuels are critically contingent on what current land

uses will be converted for feedstock expansion and how converted land will be managed. We assessed the conse-

quences of land use and land management for the agroindustrial production of sugarcane to the physical, chemi-

cal, and biological properties of freshwater systems. We surveyed 16 environmental variables and algae, tadpoles,

predatory invertebrates, and ﬁsh in lentic water bodies distributed across a gradient in land-use intensity ranging

from seasonal Atlantic Forest and cerrado to pastures to sugarcane plantations in SE Brazil, the most important

sugarcane-producing region in the world. The gradient in land-use intensity was not only an axis of native habitat

loss but also of ecosystem productivity, as indicated by increased conductivity, turbidity, and phytoplankton bio-

mass. Land use had a clear signal on community and metacommunity organization, with converted land being

impoverished in biodiversity relative to native habitats. However, frequency of occurrence, density, biomass, and

alpha diversity of tadpoles and their predators were not affected by land use. These results suggest that sugarcane

ﬁelds function as habitat to a fraction of aquatic biodiversity. Within sugarcane ﬁelds, larger wetlands surrounded

by buffer strips as required by law appeared comparatively buffered against land management practices and

housed a disproportional fraction of animal biomass, likely acting as sources of migrants to other water bodies in

the landscape. Conversion of pastures to sugarcane ﬁelds, suggested as a strategy to reduce competition for land

with food production and biodiversity conservation, does not appear to have strong consequences to lentic fresh-

water systems, provided that wetlands and surrounding buffer strips are preserved. These observations empha-

size the importance of enforcement of legislation regulating land use (i.e. the ‘Forest Code’) and certiﬁcation

systems verifying compliance and rewarding the voluntary adoption of better land management practices.

Keywords: agriculture, Atlantic Forest, cerrado, C

odigo Florestal, conservation, ethanol, frog, land-use change, metacommunity,

pasture

Received 19 February 2015 and accepted 25 March 2015

Introduction

Global energy demand is predicted to rise by 37% from

2012 to 2040 and, despite the continuing predominance

of fossil fuels, consumption of biofuels for transporta-

tion is to be increased more than threefold (IEA, 2014).

Biofuels are expected to alleviate human reliance on

nonrenewable fossil fuels while contributing to a reduc-

tion in greenhouse gas emissions and to the promotion

of rural development. However, the environmental ben-

eﬁts of biofuels are critically contingent on which,

where, and how biofuel feedstocks are produced. This

occurs because feedstocks vary broadly in energetic efﬁ-

ciency, because their expansion may promote the con-

version of lands of high conservation value and release

large quantities of stored carbon, and because intensive

agriculture is linked to various forms of environmental

degradation (OECD, 2001, 2006; Clay, 2004; Fargione

et al., 2008; Lapola et al., 2010).

Sugarcane is the most energetically efﬁcient ﬁrst-gen-

eration source of ethanol, yielding over eight units of

biofuel energy output per-unit energy input when com-

pared with two for beet, wheat, or corn (WWI, 2006).

Echoing a global expansion of biofuel crops, between

2002 and 2012 sugarcane land cover in Brazil almost

doubled to reach a total of 9.7 million hectares, and it

has to expand another 1.4–4.3 million hectares if the

country is to reach its 2020 ethanol production goals

(UNICA, 2008; Lapola et al., 2010). Brazil currently

responds to 35% of all sugarcane produced in the

world, half of which concentrated in southeastern state

of S~

ao Paulo (UNICA, 2014).

Despite signiﬁcant recent advances, sugarcane produc-

tion in Brazil has been historically associated with seri-

ous environmental impacts. These include deforestation

Correspondence: Luis Schiesari, tel. +55 11 992346740, fax +55 11

30918120, e-mails: lschiesa@usp.br; lschiesari@gmail.com

This is an open access article under the terms of the Creative Commons Attribution License,

which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 1

GCB Bioenergy (2015), doi: 10.1111/gcbb.12279

of the Atlantic Forest and to a lesser extent the cerrado,

large-scale preharvest burns, extensive soil erosion, high

water consumption in mills, and deliberate release of

vinasse in streams and rivers causing eutrophication,

algal blooms, anoxia, and ﬁsh kills (Dean, 1997; Ballester

et al., 1999; Gunkel et al., 2007; Martinelli & Filoso, 2008).

In addition, sugarcane production has a signiﬁcant

potential for environmental contamination from the

moderately high consumption of inorganic and organic

fertilizers (Cantarella & Rossetto, 2010; UNICA, 2011),

and the moderate consumption of a broad range of pesti-

cides (225 formulations containing 62 active ingredients;

Schiesari & Grillitsch, 2011).

Perhaps surprisingly then, explicit assessments of the

impacts of sugarcane production on biodiversity are

rare. For example, a recent review of the impacts of

global biofuel crop production on biodiversity failed to

ﬁnd a single article on sugarcane (Immerzeel et al., 2014;

but see, e.g. Corbi et al., 2008; Verdade et al., 2012).

Freshwater systems constitute an appropriate system

to assess the effects of land use and land management

on biodiversity because are intimately connected to sur-

rounding terrestrial systems by the transfer of energy

and matter. Furthermore, water bodies usually sustain

diverse communities comprising species with varying

degrees of dependence on the aquatic environment.

Whereas many species are obligate aquatic, many others

have complex life cycles and as such integrate the

cumulative effects of freshwater and terrestrial degrada-

tion over the course of their life history. Finally, there is

a solid tradition in freshwater theoretical and applied

ecology that can provide a basis for interpreting land-

use effects on traits, individuals, populations, and com-

munities (e.g. Wetzel, 2001).

This study aimed at assessing the consequences of land

use and land management for the production of sugar-

cane on the physical, chemical, and biological properties

of freshwater systems, with an emphasis on the diversity,

composition, and structure of their communities.

This assessment was based on sampling surveys in

replicated lentic (i.e. still) water bodies distributed across

a gradient in land-use intensity ranging from seasonal

Atlantic Forest, wooded cerrado (‘cerrad~

ao’) and cerrado

to pastures to sugarcane plantations in the state of S~

Paulo, and employing amphibian larvae and their preda-

tors as the study system. The sampling design thus cap-

tures three types of land conversion associated with the

historical expansion of sugarcane: the conversion of

native habitats to pasture, the conversion of native habi-

tats to sugarcane, and the conversion of pasture to sugar-

cane (Dean, 1997). The latter, in particular, is central in

the debate regarding the current and future expansion of

biofuel crops in the country. A recently approved

agroecological zoning for the sustainable production of

sugarcane identiﬁed as suitable 37 Mha currently

covered by low-proﬁtability pastures and concluded that

sugarcane expansion could occur over pastures with no

impacts on land covered by native vegetation or devoted

to food production (Manzatto et al., 2009; Federal decree

6961/2009). Other studies arrived at a similar recommen-

dation while targeting at a reduction in carbon emissions

(Lapola et al., 2010). Therefore, considering that indus-

trial scale sugarcane production follows an intensive

model of agriculture, this raises the question not only of

the environmental impacts of sugarcane production rela-

tive to native habitats, but also relative to pastures,

which may support moderate levels of biodiversity.

Materials and methods

Study site

Field work was conducted in the Estac

ao Ecol

ogica do Jata

(EEJ) and surrounding farms in the municipality of Luis Anto-

nio, S~

ao Paulo, southeastern Brazil (21°3401100S, 47°4400700W).

The EEJ represents one of the very few preserved (mostly sec-

ond growth) remnants of cerrado, wooded cerrado (‘cerrad~

ao’),

and seasonal Atlantic Forest vegetation in the state of S~

ao Paulo,

and is embedded in a matrix largely dominated by intensive

sugarcane cultivation, with a smaller occurrence of pastures

and silviculture. Around the EEJ, we were granted access to two

farms cultivating sugarcane in industrial scale and one small

ranch raising cattle and sheep. According to local agronomists,

land management for sugarcane production in these farms are

typical for the broader region of Ribeir~

ao Preto, which is the

most traditional sugarcane-producing region in the country.

Selection of water bodies

We selected 15 lentic water bodies in native habitats, 15 in pas-

tures, and 17 in sugarcane ﬁelds based on the following crite-

ria: (i) that the water body was amenable to pipe sampling,

that is, that a considerable fraction of the water body was less

than 60 cm deep; (ii) that the water body in a given land-use

type was at least 100 m away from another land-use type; (iii)

that the water body was independent from and at least 50 m

away from other sampled water bodies; (iv) that each land-use

type included temporary, semipermanent, and permanent

water bodies, given the importance of hydroperiod in inﬂuenc-

ing freshwater community composition (Wellborn et al., 1996).

Water bodies comprised puddles, ditches, ponds, farm ponds

(‘cacimbas’), reservoirs, swamps, and marshes varying in size

from 1.4 to 106 000 m

(see Fig. 1). Not all of the selected water

bodies were available for each analysis because some were dry

or did not contain tadpoles at the moment of sampling.

Sampling protocol

Selected water bodies were inspected monthly from December

2010 to November 2011 for phenological record and measure-

ment of water depth for estimation of hydroperiod (% of the

2L. SCHIESARI & D. T. CORR

monthly visits in which water depth >0 cm). In December 2010

and February 2011, respectively, at the beginning and middle of

the rainy season, water bodies were subject to comprehensive

habitat and physicochemical characterization, amphibian calling

surveys, and freshwater community surveys. Timing of sampling

surveys in this seasonal landscape was chosen based on the phe-

nology of occurrence of water bodies (two-thirds of which only

existed in the rainiest months) and their communities.

Physical and chemical characterization of water bodies

Prior to the community sampling surveys, we conducted a

comprehensive characterization of water bodies. Habitat

characterization comprised recording spatial positioning, land-

use type, any ongoing activities of land management, water

body dimensions, canopy cover over the pond basin (in %,

with a spherical crown densiometer; Forestry Suppliers, Jack-

son, MS, USA), substrate type (rocks, pebbles, sand, clay, mud,

wood, leaf-litter) and cover (each substrate type categorized as

comprising 0–24%, 25–49%, 50–74%, 75–100% of the pond

basin), aquatic vegetation type (i.e. terrestrial/paludicolous

plants, ﬂoating macrophytes, submerged macrophytes) and

cover (as above), and a description of the surrounding terres-

trial vegetation. We then quantiﬁed in situ basic physicochemi-

cal water parameters including temperature, pH, conductivity

(with an Orion 3-star pH meter and an Orion 3-star conductiv-

ity meter; Thermo Scientiﬁc, Waltham, MA, USA), and dis-

solved oxygen (henceforth DO; with a YSI Pro20 DO meter;

Fig. 1 Effects of land use on selected environmental variables related to water body structure (left), water physicochemistry (middle)

and productivity (right). See Table S1 for univariate statistical analyses. Data from both sampling surveys are lumped for each

response variable. Because in each land-use water bodies were selected so as to cover the full spectrum of the hydroperiod gradient,

the inclusion of area and hydroperiod in this ﬁgure is meant to demonstrate that this important gradient was controlled in our sam-

pling surveys. Corrected a=0.002.

SUGARCANE PRODUCTION AND BIODIVERSITY 3

Yellow Springs, OH, USA), as well as turbidity (with an AQ

4500 Advanced Aquafast IV Turbidimeter; Thermo Scientiﬁc,

Waltham, MA, USA) and phytoplankton standing crop (in trip-

licate, with an Aquaﬂuor Handheld Fluorometer with in vivo

chlorophyll-aand phycocyanin channels; Turner Designs, Sun-

nyvale, CA, USA). We also collected and preserved water sam-

ples for laboratory analyses of water hardness, total nitrogen

(TN), and total phosphorus (TP). These parameters were ana-

lyzed with a HACH DR 2800 spectrophotometer and appropri-

ate reagent kits (HACH, Loveland, CO, USA).

Calling activity of amphibians

Prior to the freshwater community sampling surveys, we

recorded in each water body the calling activity of amphibian

adults to provide a more comprehensive assessment of

amphibian community composition, to assess the efﬁciency in

larval sampling, and to aid in larval identiﬁcation. Calling sur-

veys were semiquantitative (i.e. in the following categories of

abundance: 0, 1–2, 3–5, 6–10, 11–20, 21–50, or more than 50 call-

ing individuals; Heyer et al., 1994) and conducted for a total of

2–4 nights in each water body.

Freshwater communities

We sampled the fauna of tadpoles and their predators, namely

nymphal dragonﬂies (Odonata: Aeshnidae, Libellulidae, Cor-

duliidae, Gomphidae), adult and larval beetles (Coleoptera: Dy-

tiscidae, Hydrophylidae), adult and nymphal heteropterans

(Heteroptera: Notonectidae, Belostomatidae, Nepidae), and

ﬁshes.

Samples were taken by pipe sampling, dipnetting, and sein-

ing (e.g. Heyer et al., 1994; Werner et al., 2007). Pipe sampling

provided quantitative per-unit-area information on species

composition, abundances, and biomass. Pipes were 60 cm tall

and 33 cm in diameter and therefore sampled 0.09 m

of water

body habitat. The sample was taken by quickly thrusting the

pipe through the water column and into the sediments to seal

the sample area. We then removed by dipnetting all animals

>5 mm from the sampled water column and the ﬁrst centime-

ter of the sediments. In practice, we considered the pipe to be

empty when at least 10 consecutive sweeps were made without

capturing any more animals. Sampling effort was scaled to

pond surface area: Five pipes were sampled in water bodies

<10 m

, 15 pipes in water bodies >10 m

and <50 m

, 30 pipes

in water bodies >50 and <200 m

, 60 pipes in water bodies

>200 m

and <500 m

and 90 pipes in water bodies >500 m

Pipes were distributed so as to representatively sample all mi-

crohabitats in a water body. In water bodies with deeper

waters (i.e., deeper than sampling pipes; NAT01, NAT05,

PAS09, SUG08, SUG09), we supplemented pipe sampling with

three hauls of a 10-m seine in the deeper water. Tadpoles and

ﬁshes were immediately euthanized and preserved in 10% buf-

fered formalin, invertebrates in 70% ethanol.

In the laboratory, all biological samples were sorted and

identiﬁed to family (invertebrates) or species level (vertebrates),

except for the amphibians Scinax and Rhinella, which were

assigned to genus only because could not be conﬁdently

assigned to species (at our study site, there are two species in

the genus Scinax,S. fuscovarius and S. similis, and two in the

genus Rhinella,R. ornata and R. schneideri), counted and

weighed. Fishes with detritivorous or herbivorous feeding hab-

its were excluded from the analysis. Summarizing, in each

water body we obtained as biological response variables com-

munity composition, species or family richness, densities, and

per-unit area biomasses of tadpoles and predators.

Data analyses

Effects of land use on environmental and biological vari-

ables. We ﬁrst conducted two-way analyses of variance fol-

lowed by Tukey HSD post hoc tests for testing the effects of

land use, survey (i.e. whether in the beginning or middle of the

rainy season), and a land-use-by-survey interaction term on

each individual variable. The effects of survey could not be

assessed for hydroperiod as this is a year-round summary met-

ric, and for conductivity and TN, as these variables were quan-

tiﬁed in the ﬁrst survey only due to technical issues. In all

other cases, a land-use-by-survey interaction term was found

nonsigniﬁcant and was dropped from the analysis. When the

assumptions of normality and homogeneity of variances could

not be met even after transformations, we employed Kruskal–

Wallis nonparametric tests followed by pairwise comparisons.

In all cases, we applied Bonferroni corrections to avoid Type I

error inﬂation.

We then conducted two separate permutational multivariate

analyses of variance (perMANOVA) to test for multivariate land-

use differences in the environmental and community datasets.

PerMANOVAs were run on the Euclidean distances of the log-

transformed environmental data (Anderson et al., 2006) and on

the Bray–Curtis distances of the Hellinger-transformed tadpole

species density data (Legendre & Gallagher, 2001). Both trans-

formations were implemented in the function decostand of the

R package vegan (Oksanen et al., 2012). The homogeneity of

variances among groups was checked previously to the perMA-

NOVA using the function betadisper from the R package vegan

(Oksanen et al., 2012). When signiﬁcant differences among

land-use types were detected, we ran multiple comparisons

with Bonferroni-adjusted signiﬁcance levels. R version 2.15.2 (R

Core Team, 2012) was used in all statistical analyses.

Alpha, beta, and gamma diversity. We compared alpha diver-

sity among land-use types by an analysis of variance on the

total number of larval amphibian species, or predator families,

observed in each water body. We also compared amphibian

beta diversity among water bodies within each land-use type

using the procedure proposed by Baselga (2010, 2012) and

implemented in the R package betapart (Baselga & Orme, 2012).

This procedure decomposes the overall beta diversity (b

SOR

)

into two components: (i) spatial turnover (b

SIM

), which is the

fraction due to replacement of some species by others along the

sites, and (ii) nestedness (b

NES

), which is the fraction due to dif-

ference in species richness, such as sites with lower richness

being a subset of the richest site (Baselga, 2010, 2012). To test

the difference between beta diversity components, we used a

resampling procedure where we took 1000 random samples of

4L. SCHIESARI & D. T. CORR

ﬁve sites per area and calculated the average b-values. With

the estimated distribution of bvalues, we assessed the

between-area signiﬁcance by calculating the probability of the

area with smaller b-value being larger than the other just by

chance (Baselga, 2010). We decided not to compare predator

beta diversity within each land-use type because of the difﬁ-

culty in interpreting this metric at such a crude taxonomic (i.e.

family) level. We compared gamma diversity among land-use

types by rarefaction curves extrapolating species richness in

each land-use type to 11 samples, that is, the maximum num-

ber of water bodies sampled in a given land-use type (Colwell

et al., 2012). Rarefaction was performed using the software ESTI-

MATES (Colwell, 2013).

Predictors of amphibian species richness. To assess what fac-

tors inﬂuence local amphibian species richness (i.e. alpha diver-

sity), we performed a generalized linear model (GLM) with a

model selection and model averaging approach considering

land use and seven variables recognized in the literature as

inﬂuencing tadpole richness. These were water body area, hy-

droperiod, canopy cover, the presence of ﬁsh, predator density,

competitor density, and distance to forest edge (Wellborn et al.,

1996; Werner et al., 2007). Quantitative variables ranged over

several orders of magnitude and were log-transformed prior to

the analysis (Anderson et al., 2006) using the function deco-

stand of the R package vegan (Oksanen et al., 2012). We assessed

the occurrence of multicollinearity among quantitative variables

by the variance inﬂation factor (VIF). All VIFs were below the

suggested threshold (VIF <3; Zuur et al., 2009, 2010). We ﬁtted

a global model to the data using a Poisson distribution (no

overdispersion detected). The global model contained all eight

explanatory variables and from that model we generated a set

with all possible submodels using the function dredge from the

R package MuMIn (Barton, 2012). We decided to run all possi-

ble models as we a priori selected only variables known to inﬂu-

ence amphibian richness. We employed Akaike’s information

criterion corrected for small sample sizes (AICc) to rank the

obtained models and selected models with ΔAICc <2 (Burn-

ham & Anderson, 2002) to compute the model-averaged param-

eters using the function model.avg in MuMIn package (Barton,

2012). We did the model averaging with shrinkage, where in

models where a variable is absent its coefﬁcient is set to zero

(Burnham & Anderson, 2002). We also assessed the likelihood

of the models using Akaike weights, which indicates how likely

the model is the best among the ones considered.

Community structure, land use, and associated environmen-

tal variables. To determine the exclusive and shared effects of

environmental variables and land use on community structure

we conducted redundancy analyses (RDA) using the variation

partitioning method with adjusted R

following Borcard et al.

(2011). To objectively reduce dimensionality while maintaining

interpretability, we ﬁrst separated the 18 environmental vari-

ables in structural properties (area, depth, hydroperiod, canopy,

vegetation cover, organic sediment cover), basic physicochemi-

cal water properties (temperature, pH, DO, conductivity, tur-

bidity, hardness), properties related to ecosystem productivity

(total nitrogen, total phosphorus, chlorophyll-a concentration,

phycocyanin concentration), and predation pressure (density of

ﬁsh, density of predatory invertebrates). We ran one PCA on

each of these groups and retained the site scores of the ﬁrst and

second axes as explanatory environmental variables.

Tadpole density and environmental variables were, respec-

tively, subject to the Hellinger (Legendre & Gallagher, 2001)

and log-transformation (Anderson et al., 2006), both imple-

mented in the function decostand of the R package vegan (Ok-

sanen et al., 2012). We selected the environmental variables to

be used in the variation partitioning by a forward selection

method (Blanchet et al., 2008; Borcard et al., 2011). We tested by

a permutation test with 999 permutations (Borcard et al., 2011)

the signiﬁcance of the testable fractions of the explanatory vari-

ables in the variation partitioning. All analyses were performed

in the R package vegan (Oksanen et al., 2012).

Analyses using the ﬁrst and the second sampling surveys,

and a summary dataset comprising both surveys had similar

results. Therefore, we present here only the analyses with the

summary dataset. The summary environmental explanatory

matrix was constructed using the average values of the two

surveys for variables and water bodies sampled in both sur-

veys; the only value available for variables or water bodies

sampled in a single survey; and the maximum density of inver-

tebrate and ﬁsh predators across surveys. The summary com-

munity matrix was constructed using the maximum density of

each tadpole species per-pond across surveys.

Metacommunity structure, land use, and associated environ-

mental variables. To analyze the structure of the amphibian

metacommunity, we ﬁrst summarized the distribution pattern

of 21 amphibian species in 26 water bodies (three additional

water bodies were excluded for not containing amphibians) by

an incidence matrix representing the site-by-species presence/

absence data. For completeness, we included both calling sur-

vey and tadpole survey data in this incidence matrix; analyses

of an incidence matrix comprising only tadpole survey data

yielded qualitatively similar results.

We tested whether incidences differed from a null model of

random placement of species in water bodies by ordering rows

and columns of the incidence matrix by reciprocal averaging

(i.e. correspondence analysis), such that water bodies with the

most similar species lists and species with the most similar dis-

tributions were closest together. We then tested this ordinated

matrix for its coherence, that is, whether embedded absences

within species distributions were signiﬁcantly less common

than expected by chance, using the null model randomization

method r0 (Presley et al., 2010). Signiﬁcant coherence implies

that there is a strong axis of variation in metacommunity struc-

ture, and justiﬁes further characterization of elements of meta-

community structure in terms of species turnover or nested

subsets, and if there is a signiﬁcant degree of boundary clump-

ing among species distributions (Leibold & Mikkelson, 2002).

Altogether, these analyses permit testing whether our incidence

matrix ﬁts one of the several idealized patterns of metacommu-

nity structure (Clemmentsian vs Gleasonian gradients, nested

subsets, evenly spaced, checkerboards), which could in some

cases provide insights into hypothesized underlying structur-

ing mechanisms.

SUGARCANE PRODUCTION AND BIODIVERSITY 5

We performed Spearman rank correlations between site ordi-

nation scores and site richness and site environmental variables

to interpret the axis of environmental variation associated with

the latent gradient (as in Meynard et al., 2013) and tested by

means of an ANOVA on site ordination scores whether land use

signiﬁcantly inﬂuences community arrangement along the ordi-

nation axes.

Analyses were conducted following the methodology pro-

posed by Leibold & Mikkelson (2002), modiﬁed by Presley

et al. (2010) using R package metacom (Dallas, 2014).

Results

Land-use patterns of environmental properties of water

bodies

Land use had a signiﬁcant univariate effect on seven of

18 measured environmental variables. These were can-

opy cover, temperature, conductivity, turbidity, water

hardness, and chlorophyll-aand phycocyanin concen-

trations (Fig. 1, Table S1). Among the three forms of

land use, water bodies in native habitats had the lowest

turbidity, water hardness, and phycocyanin concentra-

tions. In turn, water bodies in sugarcane plantations

had the highest temperatures and chlorophyll-aconcen-

trations. The only distinctive characteristic of water

bodies in pastures were the lowest temperatures. Irre-

spective of land use, a signiﬁcant effect of survey was

detected for chlorophyll-aconcentration (greater in

December), and for TP and phycocyanin concentration

(greater in February).

Land use also had a signiﬁcant effect on the environ-

mental properties of water bodies considered jointly

(perMANOVA,F

2,31

=6.68, P<0.01; Fig. 2). Environmen-

tal properties of water bodies in native habitats were

signiﬁcantly different both from those in sugarcane

plantations (perMANOVA,F

1,24

=13.27, adj. P<0.01) and

pastures (perMANOVA,F

1,17

=4.11, adj. P=0.02), which

could not be differentiated from each other (perMANOVA,

1,21

=1.86, adj. P=0.33).

Land-use patterns of amphibians and their predators

Most water bodies in all three forms of land use con-

tained amphibians and their predators (Fig. 3a). Tad-

poles were found in 70% of the water bodies sampled

in native habitats, but in 100% of the water bodies sam-

pled in pastures and sugarcane ﬁelds. In turn, predators

were found in 100% of the water bodies sampled in

native habitats and pastures, but in 70% of the water

bodies sampled in sugarcane ﬁelds. Interestingly, land

use had no univariate effect on the density and per-unit

area biomass of tadpoles or of their predators (Fig. 3b,c,

Table S1).

Although the three water bodies with the highest

amphibian species richness were all found in native hab-

itats (12, 10 and 7 species), and although the richest

water bodies in pastures and sugarcane ﬁelds had half

as many species (6 species), no signiﬁcant univariate

effect of land use on amphibian species richness was

detected either (Fig. 3d, Table S1). This occurred because

of the high among-pond variability in amphibian species

richness in all three land-use types (0–12 species in

native habitats, 2–6 in pastures, and 1–6 in sugarcane

ﬁelds). Likewise, the overall amphibian beta diversity

SOR

) and its two components, spatial turnover (b

SIM

)

and nestedness (b

NES

), were similar among land use

–0.10 –0.05 0.00 0.05

–0.06 –0.02 0.02 0.06

Environment

NMDS1

NMDS2

–1 0 1 2

–1.0 –0.5 0.0 0.5 1.0

Tadpoles

NMDS1

NMDS2

Fig. 2 nMDS plots of the environmental (left) and tadpole community (right) data from water bodies distributed across a gradient in

land-use intensity comprising native habitats, pastures, and sugarcane plantations. Black triangles =sugarcane plantations, gray

squares =pasture, open circles =native habitats. Environment plot based on the Euclidian distance of 16 log-transformed environ-

mental variables. Stress value =0.153. Tadpoles plot based on the Bray–Curtis distance of 21 tadpole species Hellinger-transformed

density data. Stress value =0.082.

6L. SCHIESARI & D. T. CORR

types (mean b

SOR

SIM

, and b

NES

were 0.71, 0.42, 0.29 for

native habitats, 0.69, 0.49, 0.20 for pastures, and 0.69,

0.51, 0.18 for sugarcane; P>0.05 for all land use compar-

isons). In contrast, gamma diversity differed among

land-use types. Total measured amphibian richness was

17 species in native habitats, 8 in pastures, and 10 in sug-

arcane ﬁelds (Fig. 3e). Correspondingly, extrapolation of

rarefaction curves of species richness to 11 samples, that

is, the maximum number of water bodies sampled per

land-use type, indicated that species richness in native

habitats (mean 17.62, 95% CI 13.45–21.79) was signiﬁ-

cantly higher than species richness in pastures (8.68,

6.24–11.12) and sugarcane ﬁelds (10, 8.71–11.29), which,

in turn, did not differ from each other.

While the analysis of patterns of predator diversity

should be exercised with caution due to the crude taxo-

nomic resolution, no univariate effects of land use on

the per-pond number of predator families were detected

(Fig. 3d; Table S1). Overall, the number of predator fam-

ilies declined from preserved to converted landscapes

(Fig. 3e), but this occurred exclusively due to ﬁsh,

which were more common in native habitats because of

three water bodies seasonally linked to streams.

Predictors of amphibian species richness

From the set of models generated to infer the best com-

bination of environmental variables predicting amphib-

ian species richness, ﬁve models were best supported

(ﬁve models had DAICc <2; Table 1, Table S2). Hydro-

period and tadpole density were present in all ﬁve top

models, and therefore, were assigned a relative impor-

tance of 1.00 after model averaging (Table 1). Tadpole

species richness increased with tadpole density and hy-

droperiod, that is, water bodies that contained more

tadpoles per-unit area and that held water for longer

(a)

(b)

(c)

(d)

(e)

Fig. 3 (a) Frequency of occurrence (b) Density (c) Per-unit-

area biomass (d) Richness per pond and (e) Richness per land-

use type of tadpoles (left) and predators (right) in water bodies

distributed across a gradient in land-use intensity comprising

native habitats, pastures, and sugarcane plantations. Here fre-

quency of occurrence refers to the % of water bodies that con-

tained tadpoles or predators in either the ﬁrst (December) or

second (February) community surveys. Density and per-unit-

area biomass boxplots lump data from both surveys, and rich-

ness per pond and richness per land-use type consider the

cumulative species list found in a given pond (or land use)

across surveys. Richness for amphibians is species richness, for

invertebrates (which include dragonﬂies, water bugs, beetles,

and ﬁsh) is family richness. Because few ﬁsh species were cap-

tured by pipe sampling, estimates of predator richness include

ﬁsh captured by seine nets as well. Land use had a signiﬁcant

effect in (e) but not in (b), (c), or (d). See Table S1 for univariate

statistical analyses.

SUGARCANE PRODUCTION AND BIODIVERSITY 7

periods had higher tadpole richness (Fig. S1). Because

the 95% conﬁdence intervals of all other variables

included zero (Table 1), there is not enough evidence

that distance to native habitats, ﬁsh presence, and can-

opy cover affect tadpole species richness in our study.

Amphibian community structure, land use, and associated

environmental properties

As for environmental properties, land use had a signiﬁ-

cant effect on amphibian community structure (perMANO-

VA,F

2,21

=3.74, P<0.01; Fig. 2). Amphibian communities

in native habitats differed signiﬁcantly from those in sug-

arcane ﬁelds (perMANOVA,F

1,16

=4.84, adj. P=0.04),

whereas those in pastures could not be differentiated from

either of them (perMANOVA F

1,11

=2.83, adj. P=0.09 for

pasture-native habitat comparison and F

1,15

=3.31, adj.

P=0.07 for pasture-sugarcane comparison).

Land use, however, comprises several axes of envi-

ronmental change that could, alone or in combination,

inﬂuence amphibian community structure. Among the

many descriptors of freshwater habitats, the forward

selection procedure retained four composite environ-

mental variables in our approach to reduce dimension-

ality. These were the ﬁrst PCA axis of properties related

to ecosystem productivity (prod1), the ﬁrst PCA axis of

water physicochemical properties (phys_chem1), and the

ﬁrst and second PCA axes of predation pressure (pred1,

pred2) (see Table S3 and Fig. S2 for details). Axis prod1

explained 65.4% of the total among-site variation and

was positively related to TN. Chlorophyll-aand phyco-

cyanin concentrations, and TP, were weaker positive

contributors to prod1. Axis phys_chem1 explained 69.5%

of the total among-site variation and was positively

related to turbidity. Conductivity and water hardness

were weaker positive contributors to phys_chem1. Axes

pred1 and pred2 explained all total among-site variation

(57.3% and 42.7%, respectively), with pred1 being nega-

tively related to both the maximum density of predatory

invertebrates and ﬁsh, and pred2 being positively related

to the maximum density of ﬁsh but negatively related

to the maximum density of predatory invertebrates.

The above-mentioned selected composite environ-

mental variables (axes of PCA) and land use together

explained 48.6% of the total tadpole community

variability (R2

adj =0.49, P<0.01). From the total variabil-

ity, 31% was explained exclusively by the selected envi-

ronmental variables (R2

adj =0.31, P<0.01), and over

fourteen percent was explained by the shared compo-

nent between environmental variables and land use

(R2

adj =0.14, p not testable). Land-use alone explained

less than three percent of the tadpoles community vari-

ability and was not signiﬁcant (R2

adj =0.03, P=0.11).

The ﬁrst RDA axis was negatively related to phys_chem1

and pred1, and less so to prod1 and pred2 (see Table S4

and Fig. S3 for RDA site and species scores, and biplots

of individual selected composite environmental vari-

ables). Therefore, increasing score values along the ﬁrst

RDA axis, among other characteristics, described a gra-

dient ranging from water bodies with high turbidity

and TN, and less predatory invertebrates and ﬁshes

(water bodies mainly located in sugarcane ﬁelds), to

water bodies with low turbidity and TN, and more

predatory invertebrates and ﬁshes (water bodies mainly

located in native habitats and pasture). The second

RDA axis was positively related to pred1 and negatively

related to pred2 (Fig. S3). Therefore, increasing score val-

ues along the second axis described mainly a gradient

from water bodies with more predatory ﬁsh and less

predatory invertebrates to water bodies with less preda-

tory ﬁsh and more predatory invertebrates. Most spe-

cies were found in water bodies devoid of ﬁsh; the

glaring exception was the bufonid Rhinella, typically

found in water bodies with high densities of ﬁsh. Scinax

and Physalaemus cuvieri were usually related to less pro-

ductive water bodies, with lower TN and lower turbid-

ity. By contrast, Eupemphix nattereri and Leptodactylus

fuscus were usually associated to more productive water

bodies with higher TN and higher turbidity.

Amphibian metacommunity structure, land use, and

associated environmental properties

The amphibian metacommunity exhibited strong

coherence along the ﬁrst axis of ordination (z=3.21,

P<0.001; Fig. 4). There were 141 embedded absences

in a 21 926 species-by-site incidence matrix (546

cells). The community exhibited a nonsigniﬁcantly

Table 1 Model averaged estimates (with shrinkage) from the

ﬁve generalized linear models (ΔAICc <2; Table S2) predicting

tadpole species richness on 27 water bodies distributed across

a gradient in land-use intensity comprising native habitats, pas-

tures, and sugarcane plantations. SE =standard error;

CI =95% conﬁdence interval. There is a positive relationship

between hydroperiod and richness and between tadpole den-

sity and richness (intervals do not cross zero)

Variable Estimate

Adjusted

Lower

Upper

Relative

importance

(intercept) 1.260 0.73 2.29 0.17 –

Hydroperiod 0.121 0.05 0.02 0.22 1.00

Tadpole

density

0.184 0.05 0.08 0.29 1.00

Distance 0.019 0.02 0.07 0.01 0.57

Fish 0.325 0.34 1.28 0.06 0.54

Canopy

cover

0.007 0.04 0.15 0.03 0.12

8L. SCHIESARI & D. T. CORR

positive turnover (z=1.39, P=0.164) and was signif-

icantly clumped (Morisita’s index =2.559, df =18,

P<0.001). The ﬁrst axis of ordination was positively

correlated with land-use intensity, conductivity, turbid-

ity, TN, TP, chlorophyll-a, and phycocyanin concentra-

tions (Spearman rank correlation, P≤0.027) and

negatively correlated with area, hydroperiod, vegeta-

tion cover, and organic sediment cover (P≤0.017). As

hypothesized, land-use intensity had a signiﬁcant effect

on ordination scores (ANOVA F

2,26

=3.51 P=0.047): post

hoc analyses indicated that ordination scores of native

habitat communities were signiﬁcantly different from

those of sugarcane communities, whereas ordination

scores of pasture communities were not signiﬁcantly

different from either those of native habitats or of sug-

arcane plantations. Species richness was signiﬁcantly

correlated with site scores of the ﬁrst axis (Spearman

rho =0.47, P=0.016).

Discussion

Land use and land management for the production of

sugarcane had a clear signal on the physical, chemical

and biological properties of freshwater systems. In a

ISN

DOIREP

RDY

REVOCYPONAC

iidnulsa

sep

rtluc

otnodO

blasa

nsuhpos

Rhinella spp

rebafsa

uni

icidop

ulytc

dotpeL

sila

rdnoh

hasu

emo

yhP

Leptodactylus mystaceus

suc

iry

sul

Elachistocleis cesarii

Physalaemus cuvieri

Dendropsophus minutus

tatcnupoblasielcom

aihC

susol

sulahp

cyh

arT

Scinax spp

Leptodactylus fuscus

Dermatonotus muelleri

Physalaemus centralis

Eupemphix nattereri

Leptodactylus mystacinus

INTENSITY OF LAND USE, CONDUCTIVITY, TURBIDITY, CHL a, PHYCOCYANIN, TN, TP

AREA, HYDROPERIOD, VEGETATION COVER, ORGANIC SEDIMENT COVER

Fig. 4 Amphibian species-by-site incidence matrix for the Estac

ao Ecol

ogica do Jata

ı and surrounding agricultural areas. The matrix

is ordered by reciprocal averaging such that water bodies with the most similar species lists and species with the most similar distri-

butions are closest together. Position of each water body across three important freshwater environmental gradients is represented in

color coded rows at increasing shades of gray at the top of each matrix (intensity of land use: native habitats, pastures and sugarcane

plantations; hydroperiod: 0–49%, 50–99%, and 100% days with water; canopy cover: 0–33%, 34–66%, and 67–100% canopy cover).

Arrows display environmental factors signiﬁcantly associated with site ordination scores according to a Spearman rank correlation.

SUGARCANE PRODUCTION AND BIODIVERSITY 9

multivariate space deﬁned by sixteen environmental

variables, there was virtually no overlap among water

bodies in preserved land and water bodies in sugar-

cane ﬁelds. Water bodies in pastures were signiﬁ-

cantly different from those in native habitats, but not

from those in sugarcane ﬁelds. Likewise, land use

had a clear signal on community and metacommunity

organization. This signal was revealed both by guided

(i.e. nMDS and associated perMANOVA) and by

unguided ordination tools (i.e. RDA, reciprocal aver-

aging in the analysis of elements of metacommunity

structure) and emerged even after accounting for

other gradients of known importance in structuring

freshwater metacommunities such as hydroperiod,

canopy cover, and water body surface area (Wellborn

et al., 1996; Skelly et al., 1999; Werner et al., 2007).

Amphibian communities in native habitats were sig-

niﬁcantly different from those in sugarcane ﬁelds;

pastures were intermediate in community structure in

that they were not signiﬁcantly different neither from

native habitats nor from sugarcane ﬁelds. Therefore,

both abiotic and biotic data lend general support to

our hypothesis of a gradient in land-use intensity –

and therefore environmental degradation –ranging

from preserved cerrados and seasonal Atlantic Forests

to pastures to sugarcane ﬁelds.

Land-use patterns of environmental properties of water

bodies

The transition of native habitats to productive agricul-

tural land was associated with a decrease in canopy

cover and to an increase in turbidity, water hardness,

and abundance of cyanobacteria in lentic water

bodies. In turn, the transition of pastures to sugar-

cane plantations was associated with a further reduc-

tion in canopy cover, to an increase in phytoplankton

standing crop, and to a sharp increase in water con-

ductivity. Overall, the physical, chemical, and biologi-

cal characterization of water bodies indicated that, in

addition to an axis of habitat loss and fragmentation,

the gradient in land-use intensity is clearly a gradient

in ecosystem productivity. In fact, every multivariate

analysis conducted in this study strongly pointed to a

gradient in land-use intensity on indicators of produc-

tivity, especially phytoplankton standing crop. This

enhanced productivity is likely a product of increased

incident solar radiation due to canopy opening (Schie-

sari, 2006), and of the increase in nutrients from cattle

grazing and defecation in pastures, and from fertiliza-

tion in sugarcane ﬁelds. Indeed, sugarcane is an

intense consumer of fertilizers, and overuse is the

rule (Martinelli & Filoso, 2008). The likely fate of a

considerable fraction of applied nutrients is water

bodies, both by leaching (as is the case of nitrate,

which is highly soluble) and by erosion (as is the

case of phosphorus), which high rates are well docu-

mented for sugarcane and reinforced by our high

measures of turbidity and water hardness. Although

it may seem somewhat surprising that in this study

TN or TP did not show a univariate increase with

land-use intensity, 9 of the 10 highest values of TP

and of TN were found in converted land, and land-

use intensity was accompanied by a sharp increase in

water conductivity.

Land-use patterns of biodiversity

Sugarcane ﬁelds and pastures were impoverished in

amphibian biodiversity –with 10 and 9 species –rela-

tive to preserved land –with 18 species. Species sam-

pled exclusively in native habitats included Hypsiboas

faber, H. albopunctatus, H. lundii, Trachycephalus venulo-

sus, Leptodactylus labyrinthicus, L. mystaceus, Odontophry-

nus cultripes and Chiasmocleis albopunctata; in turn,

Rhinella sp. was sampled exclusively in pastures and Le-

ptodactylus mystacinus and Phyllomedusa hypochondrialis

in sugarcane ﬁelds. At least part of these land use-spe-

ciﬁc species occurrences, however, are likely sampling

effects: all species sampled exclusively in converted

land are known to occur in the Estac

ao Ecol

ogica do

Jata

ı (Prado et al., 2009, R. Sawaya pers. obs., L. Schie-

sari pers. obs.).

The amphibian metacommunity exhibited strong

coherence along the ﬁrst axis of ordination, implying

that, overall, species responded to the same environ-

mental gradient. This environmental gradient ranged

from larger water bodies with longer hydroperiods,

richer in aquatic and semiaquatic vegetation and

organic sediment, and containing water with lower

conductivity, turbidity, nutrient concentrations, and

phytoplankton standing crop, to water bodies with

the opposite characteristics. This environmental gra-

dient also ranged from water bodies embedded in

preserved landscapes to those embedded in land-

scapes with high intensity of land use that, as

hypothesized, was accompanied by decreasing spe-

cies richness.

One might expect that intensiﬁcation in land use

would be associated with a cumulative pattern of

species losses such that communities in intensively

managed landscapes would be a subset of communi-

ties in moderately intensively managed landscapes,

which, in turn, would be a subset of communities in

preserved, native habitats. In operational terms, this

would be the case if the metacommunity exhibited

positive boundary clumping and negative turnover

(Presley et al., 2010). This pattern was not strictly

10 L. SCHIESARI & D. T. CORR

observed, as we found positive boundary clumping

but positive turnover –albeit nonsigniﬁcantly so.

Such structure corresponds to a ‘quasi-Clementsian’

metacommunity structure. In a strictly Clementsian

metacommunity structure (i.e. with signiﬁcant positive

turnover), multiple species show coincident range

boundaries because of shared evolutionary history

and interdependent ecological relationships. Therefore,

groups of adjacent sites across the latent environmen-

tal gradient have shared species compositions termed

‘compartments’ (Lewinsohn et al., 2006). We identiﬁed

two compartments. The ﬁrst comprised 13–15 sites in

all land use types and across the full range of hyd-

roperiods that presented comparatively low conduc-

tivity, turbidity, and primary productivity, and up to

17 amphibian species. The second comprised eight

water bodies in converted land, characterized by

being nonpermanent, mostly devoid of vegetation,

turbid, and productive. This compartment contained

ten species including Physalaemus cuvieri, P. centralis,

Eupemphix nattereri, Dendropsophus minutus, Scinax spp,

Leptodactylus fuscus, L. mystacinus, and Dermatonotus

muelleri. Five to seven species occurred in both com-

partments.

As is frequently observed in Clementsian metacom-

munity structures, many species ranges were very

broad and had boundaries clumped at the ends of the

gradient. This could be a result either from the sam-

pled environmental gradient being too short, or from

species presenting broad niches. Considering the

remarkable breadth of lentic habitats sampled, we con-

clude that the niches of several species are indeed very

broad, including their tolerances to land-use and land

management practices. The range of Leptodactylus fus-

cus, Scinax spp (mostly S. fuscovarius), P. cuvieri and

D. minutus comprised no less than 92% (counting

embedded absences), 85%, 77%, and 73% of the latent

gradient. This is in strong contrast with species such

as Odontophrynus cultripes and Hypsiboas lundii, each

found in a single site and therefore only 4% of the gra-

dient.

In contrast to patterns in prey distributions, land use

had no effect on predatory invertebrate faunas –at

least at a crude taxonomic resolution (i.e. family level).

All three sampled bug families, all two beetle families

and two of four dragonﬂy families were found across

the gradient; the two remaining dragonﬂy families

(Corduliidae, Gomphidae) were found in at least one

converted land use type. The number of ﬁsh families

in the cerrado (8) was much larger than that in pas-

tures (4) and sugarcane ﬁelds (1), but this effect is

likely due to some water bodies in native habitats

being seasonally linked to lotic water bodies, and not

to land use.

Potential drivers of biodiversity change

Considering that most changes in community composi-

tion occurred in the transition from cerrados and sea-

sonal Atlantic Forests to pastures, and not in the

transition from pastures to sugarcane ﬁelds, it is rea-

sonable to hypothesize that habitat loss, habitat

fragmentation and habitat split –that is, the spatial

segregation between adult and larval habitat –are

important contributors to species losses in productive

land (Becker et al., 2007). Indeed, organisms with com-

plex life cycles appear to be particularly vulnerable to

land conversion not only because integrate environ-

mental degradation in aquatic habitats as larvae, and

in terrestrial habitats as juvenile and adults (each of

which alone could contribute to population declines),

but also because the spatial segregation of adult and

larval habitat obliges adults and metamorphs to risky

migrations.

Differences in land management between pastures

and sugarcane ﬁelds also are likely contributors to

changes in local species compositions and/or abun-

dances. Sugarcane ﬁelds are subject to intense physical

disturbance every year (the harvesting) and every 5–

6 years (the ﬁeld reform), plus the occasional pulses of

chemical disturbance following the application of pesti-

cides and fertilizers. Small ponds, puddles, and ditches

in sugarcane ﬁelds were typically devoid of dragonﬂy

larvae; we observed the same pattern in soybean ﬁelds,

where dragonﬂy mortality was tightly synchronized

with pesticide application (D. Negri and L. Schiesari,

pers. obs.). Some species of tadpoles were frequent and

apparently endured pesticide applications in both sug-

arcane and soybean ﬁelds, but we witnessed tadpole

dieoffs in ponds adjacent to sugarcane ﬁelds which

could plausibly be a result of pesticide application.

Indeed, Moutinho (2013) found that glyphosate, amet-

ryn, and acetochlor, three of the most common herbi-

cides applied in sugarcane ﬁelds, caused mortality of

frog larvae when manipulated at application doses rec-

ommended by the manufacturer. Likewise, ammonium

concentrations measured in ditches embedded in sugar-

cane plantations reached concentrations sufﬁcient to

cause larval amphibian mortality (Ilha & Schiesari,

2014), especially at earlier developmental stages (Bellezi

et al., 2015).

Implications for the conservation of aquatic and

semiaquatic biodiversity in managed land

Increasing environmental concerns of further conversion

of native habitats to agricultural land, and of competi-

tion between biofuel and food crops for land, led inde-

pendent researchers (e.g., Lapola et al., 2010), NGOs

SUGARCANE PRODUCTION AND BIODIVERSITY 11

(WWF, 2009) and governmental agencies (Manzatto

et al., 2009) to argue for an expansion of sugarcane over

pastures. While we agree that this is the best conserva-

tion option face to an expansion of the agroindustrial

production of biofuel feedstocks, it is nonetheless

important to acknowledge that large-scale conversion of

pastures into sugarcane ﬁelds following prevailing land

management practices is expected to lead to further ter-

restrial habitat homogenization, and increased siltation

and eutrophication of freshwater systems. Expansion of

sugarcane ﬁelds over pastures is also expected to lead

to increased environmental contamination with pesti-

cides (Schiesari & Grillitsch, 2011). Assuming conserva-

tion of wetlands and surrounding buffer strips, our data

suggest no substantial effects of further conversion of

pastures into sugarcane ﬁelds on amphibian frequency

of occurrence, density, per-unit-area biomass, and alpha

diversity. Likewise, conversion of pastures into sugar-

cane ﬁelds appears to have no effect on predator abun-

dance or per-unit-area biomass. However, a more

careful evaluation of the effects of land use on predator

alpha diversity awaits for a species-level analysis, which

is underway.

The observation that 100% and 73% of the water

bodies in sugarcane plantations contained tadpoles and

predatory invertebrates, respectively, and that tadpole

and invertebrate predator densities and per-unit-area

biomass were not affected by land use imply that (i) len-

tic freshwater habitat is limiting for organisms with com-

plex life cycles in this markedly seasonal landscape but

also that (ii) sugarcane ﬁelds are permeable to at least

part of the freshwater community. It is important to real-

ize, however, that distribution of biodiversity in sugar-

cane ﬁelds was highly uneven: three large (0.3–10.7 ha)

marshes contained 11 of the 14 species of amphibians

found in sugarcane ﬁelds, six of which found exclusively

there, and 82% of all individuals sampled. Correspond-

ingly, they contained all eight families of invertebrate

predators found in sugarcane ﬁelds, two of which found

exclusively there, and 94% of all individuals sampled.

Contrary to small ponds, farm ponds, puddles and

ditches, preservation of buffer zones around streams and

wetlands greater than 1 ha are mandated by the Forest

Code, federal legislation regulating land use in every pri-

vate property in the country. Therefore, these water

bodies were at least 30 m from sugarcane ﬁelds and, not

surprisingly, then, had less extreme abiotic characteris-

tics when compared with other water bodies embedded

in sugarcane ﬁelds, including lower turbidity, conductiv-

ity, and chlorophyll-a and phycocyanin concentrations

(Fig. S4). These larger wetlands very likely act as regional

sources of biodiversity. As an example, multiplying

organismal densities by surface area, in December 2010 a

10.7-ha marsh contained no less than ~34 million tad-

poles [31 million Scinax spp, 2.3 million Dendropsophus

minutus, and 0.5 million Physalaemus cuvieri] and ~3 mil-

lion larval insect predators [1.8 million dragonﬂies,

0.6 million bugs, 0.5 million beetles]. Part of these indi-

viduals eventually reached metamorphosis and likely

dispersed across the terrestrial environment colonizing

other water bodies in the landscape.

Another evident argument for the importance of lar-

ger wetlands as sources of biodiversity in sugarcane

ﬁelds is the observation that large-scale burnings were

until recently the standard preharvesting practice in

sugarcane ﬁelds throughout Brazil. Indeed, 43% of the

area in Luis Antonio, including part of the land sur-

rounding sampled water bodies, was burned in the year

preceding our surveys (data provided by CANASAT; Rud-

orff et al., 2010; Aguiar et al., 2011; INPE, 2014). Under

such conditions, buffered streams, streamside marshes,

and permanent and semipermanent wetlands are more

than likely important sources of biodiversity in sugar-

cane landscapes, especially to amphibians, which are at

the same time sensitive to desiccation and dispersal lim-

ited in comparison with dragonﬂies and other predatory

insects.

Whereas our observations reinforce the importance of

the Forest Code for biodiversity conservation, farmers

compliance with these the so-called Permanent Preser-

vation Areas is well below 30% in the most important

sugarcane-producing regions in the country (Sparovek

et al., 2012). Therefore, in a country with relatively

strong environmental legislation but subject to deﬁcient

enforcement, Bonsucro (Better Sugar Cane Initiative)

and any other certiﬁcation scheme that proposes to fos-

ter the sustainability of the sugarcane sector are helpful.

Bonsucro Standards demand compliance with all rele-

vant applicable laws, including the Forest Code and

those regulating the storage, delivery, and application

rates of vinasse and pesticides. Bonsucro Standards also

prevent greenﬁeld expansion over High Conservation

Value Areas and require development and implementa-

tion of an Environmental Management Plan taking into

account endangered species, habitats, and ecosystems in

the farm. Finally, Bonsucro Standards include applica-

tion of fertilizers according to soil or leaf analysis and

set a moderately restrictive maximum dosage of inor-

ganic fertilizers, pesticides, water consumption and of

tilled land area.

Considering that most native habitats in Central-

South Brazil –even if fragmented and in early phases of

regeneration –are contained within private properties,

enforcement of current legislation and recognition of

better land management practices by means of certiﬁca-

tion systems are clearly important for the conservation

of biodiversity and, more broadly, the environmental

sustainability of biofuels.

12 L. SCHIESARI & D. T. CORR

Acknowledgements

We thank the Instituto Florestal for granting permission to con-

duct research in Estac

ao Ecol

ogica do Jata

ı and farmers around

Luis Antonio for granting permission to conduct research in

their lands. We thank ICMBio and Instituto Florestal for collec-

tion permits (ICMBio 17559) and FAPESP/BIOEN –Bioenergy

Research Program (Young Researcher Award 2008/57939-9),

FAPESP/CNPq SISBIOTA Brasil Program (FAPESP 2010/

52321-7, CNPq 563075/2010-4) and CAPES (Ci^

encia sem

Fronteiras 1176/13-7) for funding. We thank Ti~

ao, Antonio Car-

los da Silva, Daniel Din Betin Negri, Mariana Fekete Moutinho,

Bianca Gonc

ßalves dos Santos, Paulo Ilha, Tiago Gabriel Correia,

and Marquinhos for ﬁeld assistance and Ana Cristina Mach-

ado, Daniel Din Betin Negri, and Ilberto Calado for lab assis-

tance. We thank Edson Montilha de Oliveira for logistical

support, Britta Grillitsch for comments in earlier phases of pro-

ject design, Mathew Leibold and his laboratory for discussion

on patterns in metacommunity structure, Denise Rossa-Feres

for sharing her expertise in tadpole identiﬁcation, Victor Gio-

vannetti and Kleber Leite for ﬁsh identiﬁcation, and Fernando

Rodrigues da Silva and Thiago Gonc

ßalves-Souza for statistical

advice.

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Supporting Information

Additional Supporting Information may be found in the online version of this article:

Table S1. Univariate analyses for the effects of land use and survey on 16 environmental variables and 8 community variables

measured in sampled water bodies.

Table S2. Top generalized linear models predicting tadpole species richness on 27 water bodies distributed across a gradient in

land use intensity comprising native habitats, pastures, and sugarcane plantations.

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sured in each water body.

Table S4. Scores from the Redundancy Analysis (RDA) of 25 larval amphibian communities in water bodies distributed across a

gradient of environmental degradation comprising native habitats, pastures and sugarcane plantations.

Figure S1. Positive relationship between tadpole richness and hydroperiod, and tadpole richness and tadpole density on 27 water

bodies distributed across a gradient in land use intensity (native habitats, pastures, and sugarcane plantations).

Figure S2. Biplots of the Principal Component Analyses used to reduce dimensionality in the 18 environmental variables mea-

sured in each water body.

Figure S3. RDA triplot of 25 larval amphibian communities in water bodies distributed across a gradient of environmental degra-

dation comprising native habitats, pastures and sugarcane plantations.

Figure S4. A comparison of representative physico-chemical properties of small and large water bodies in sugarcane ﬁelds.

14 L. SCHIESARI & D. T. CORR

Schiesari & Correa 2015 SI

Data

June 2015

Luis Schiesari · Décio Tadeu Corrêa

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Community reorganization stabilizes freshwater ecosystems in intensively managed agricultural fields

Article

Full-text available

May 2023
J APPL ECOL

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Gradients and the Structure of Neotropical Metacommunities: Effects of Disturbance, Elevation, Landscape Structure, and Biogeography

Chapter

Apr 2023

A metacommunity perspective provides ecological insight into spatiotemporal dynamics because it explicitly considers the structure and organization of communities along environmental gradients, and seeks to understand the local (e.g., biotic interactions, environmental tolerances, habitat preferences) and regional (e.g., dispersal, habitat fragmentation, landscape structure) processes that generate these patterns. More specifically, a metacommunity is a network of communities or sites that are potentially connected to each other via dispersal of individuals among constituent communities or sites. Local emigration and immigration, when coupled with other spatially explicit ecological processes such as species sorting, habitat filtering, priority effects, or interspecific competition, imbue the network with an emergent structure that corresponds to underlying environmental gradients. 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Using mesocosms to evaluate the impacts of pasture intensification and pasture-sugarcane conversion on tadpoles in Brazil

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Oct 2022
ENVIRON SCI POLLUT R

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Article

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Aug 2023

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Total nitrogen and pH are key variables for functional structure of zooplanktonic communities in an agropastoral landscape

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Changes in land use are one of the main impacts on aquatic ecosystems. The conversion of natural areas into agropastoral, such as pasture or monocultures, can affect the limnological characteristics of the water that in turn influence the structure of aquatic communities. But the impact is still unclear, particularly on zooplankton communities. The objective of this study was to evaluate the effect of water parameters from eight reservoirs inserted in an agropastoral landscape on the functional structure of zooplankton. The functional characterization of the zooplankton community was based on four traits: body size, feeding type, habitat type, and trophic group. Functional diversity indices (FRic FEve and FDiv) were estimated and modeled water parameters, using generalized additive mixed models (GAAM). The water parameters investigated were total nitrogen (TN) and total phosphorus (TP), dissolved oxygen (OD), temperature and pH. Moreover, we used RDA to analyze the influence of these environmental variables on the sharing of traits among the sample sites. FRic was high in the reservoirs with low TN concentration and low pH values. FEve was also high in low pH and high TP concentration. FDiv was high with unsharp increases of pH and high concentrations of TN and DO. Our analyses showed pH as a key variable for functional diversity, since it was related to the variation in all indices. Data also pointed out changes in diversity functional with small pH changes. The big and medium size, raptorial-cop and filtration-clad functional traits were positively associated with high concentrations of TN and alkaline pH. The small size and filtration-rot were negatively associated with high concentrations of TN and alkaline pH. Density of filtration-rot was lower in pasture landscapes. In conclusion, our study indicated that pH and TN are key variables for the functional structure of zooplanktonic communities in an agropastoral landscape.

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Growing a fin: wetland and upland effects on tadpole morphology of Scinax squalirostris (Anura: Hylidae)

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Jun 2022
ZOOMORPHOLOGY

Geographical patterns of phenotypic variation are the outcome of a complex array of evolutionary and environmental factors. Studies on the correlates of the geographic variation in morphological characters can be useful to understand the drivers of phenotypic differences and because intraspecific variation in morphology can impact either local adaptation of any given species or higher-level ecosystem processes. The morphology of larval amphibians responds to multiple factors, including wetland level and surrounding land use. However, understanding the relative influence of such environmental factors on the morphology of tadpoles remains challenging. We used geometric morphometrics to describe the intraspecific morphological variation in tadpoles of Scinax squalirostris (Anura: Hylidae) in freshwater wetlands ranging along the transition between the Pampa and Atlantic Forest biomes in southern Brazil. Specifically, we assessed the relative influence of spatial and environmental (aquatic predators, water chemistry and hydroperiod, crop area) factors to tadpole body size and shape. The size of S. squalirostris tadpoles was affected by spatial factors and pH. Smaller-sized tadpoles were observed in the Pampa–Atlantic Forest transition. Allometry-free changes in the shape of tadpoles were associated both to wetland and upland factors. Tadpoles in larger ponds showed globular bodies and higher ventral fins, while tadpoles in ponds with higher electrical conductivity showed smaller tails. Tadpoles in ponds surrounded by larger crop areas showed longer fins. Our results are useful to understand the importance of wetland and upland effects on the morphology of widely distributed aquatic species, especially given the ongoing scenarios of land cover modification and climate change.

Community variability in pond metacommunities: interactive effects of predators and isolation on stochastic community assembly

Article

Full-text available

Mar 2022

In the absence of environmental heterogeneity, spatial variation among local communities can be mostly attributed to random dispersal, demographic stochasticity and species interactions causing historical contingency in colonization (e.g. priority effects). The consequences of demographic stochasticity and random dispersal are highly dependent on community size, regional richness and local richness, which, along with historical contingency can be strongly affected by spatial isolation and the presence of predators. Here, we tested whether and how the presence of a generalist predatory fish and spatial isolation can change spatial community variability in artificial ponds by manipulating the presence/absence of fish (redbreast tilapia) at three different distances from a source wetland. We then used null models to compute how much the observed community variability within treatments deviates from the expected from randomly reassembled communities (i.e. beta‐deviation). We found that spatial isolation can have both negative and positive effects on community variability, and their importance may depend on the presence of predatory fish. Negative effects likely occurred because predatory insects cannot always successfully colonize highly isolated ponds, causing the abundance of herbivores and detritivores to increase, consequently increasing community size, which is known to decrease the importance of demographic stochasticity. However, when fish are absent, the more isolated communities exhibit more community variability than is expected from random community assembly. We believe that such an increase in variability is most likely due to an increase in the importance of historical contingency in colonization, generating more distinct communities in isolated ponds. Such effects were absent in the presence of generalist predatory fish, likely because fish prevented any early colonizing taxa from becoming too abundant. Our findings show that the presence of generalist predators can change how community variability responds to spatial isolation.

Realistic exposure to fipronil, 2,4-D, vinasse and their mixtures impair larval amphibian physiology

Article

Jan 2022
ENVIRON POLLUT

Expansion of sugarcane crops may have contributed to the increased contamination of native habitats in Brazil. Several species of amphibians inhabit ponds formed in flooded farmlands, where pesticide concentrations are usually high. This study evaluated the ecotoxicological effects of the sugarcane pesticides fipronil and 2,4-D, as well as the fertilizer vinasse (isolated and mixed), on physiological responses of Leptodactylus fuscus and Lithobates catesbeianus tadpoles. In situ assays were conducted in mesocosms with concentrations based on the doses recommended by the manufacturer. Vinasse (1.3% dilution) caused 100% tadpoles’ mortality immediately after its application. Fipronil and/or 2,4-D altered antioxidant and biotransformation responses, induced neurotoxicity and changed lipid contents in tadpoles. A multivariate approach indicated that the mixture of pesticides induced most of the sublethal effects in both tadpole species, in addition to the isolated fipronil in L. fuscus. Fipronil alone increased glucose-6-phosphate dehydrogenase (G6PDH) activity, decreased acetylcholinesterase (AChE) and total lipid contents, and altered some individual lipid classes (e.g., free fatty acids and acetone-mobile polar lipids) in L. fuscus. The interaction between fipronil and 2,4-D in this species were more evident for lipid contents, although enzymatic alterations in G6PDH, AChE and glutathione-S-transferase (GST) were also observed. In L. catesbeianus, the mixture of pesticides reduced triglycerides and total lipids, as well as increased GST and decreased AChE activities. The detoxifying enzyme carboxylesterase was reduced by 2,4-D (alone or in mixture) in both species. Isolated pesticides also modulated specific lipid classes, suggesting their disruptive action on energy metabolism of tadpoles. Our study showed that fipronil, 2,4-D, and vinasse, individually or mixed, can be harmful to amphibians during their larval phase, causing mortality or impairing their functional responses.

From genes to ecosystems: a synthesis of amphibian biodiversity research in Brazil Thematic Review

Article

Full-text available

Jan 2022

Here, we summarize examples of significant advances in amphibian research supported by the São Paulo Research Foundation (FAPESP), focusing on recent discoveries in the fields of community ecology, habitat change, infection diseases, and multipurpose DNA sequencing. We demonstrated that FAPESP has been fundamental not only by directly funding research projects and scholarships, but also through its science training policy, fostering international collaborations with world-class research institutions, improving and consolidating new lines of research that often depended on a synergetic combination of different knowledge and complex tools. We emphasized that future studies will continue to focus on basic questions, such as description of new species, as well as taxonomic and systematic corrections. Furthermore, we also expect that there will be a strong integration among different disciplines using novel bioinformatics tools and modeling approaches, such as machine learning. These new approaches will be critical to further develop our understanding of foundational questions of amphibian life-history trait variation, disease transmission, community assembly, biogeography, and population forecasts under different global change scenarios such as agricultural expansion, agrochemical use, habitat loss, and climate change.

Long‐Term Distributional Dynamics Of A Michigan Amphibian Assemblage

Article

Full-text available

Oct 1999

http://deepblue.lib.umich.edu/bitstream/2027.42/117066/1/ecy19998072326.pdf

Ontogenetic Variation in the Sensitivity of the Gladiator Frog, Hypsiboas faber, to Inorganic Nitrogen

Article

Full-text available

Feb 2015
COPEIA

In a biosphere transformed by human activities, understanding the relationship between age, developmental stage, or body mass and toxicological sensitivity is a relevant endeavor because the environmental release of some quantitatively important contaminants follows predictable seasonal patterns, as do wildlife demographic events. We tested the hypothesis that the sensitivity of the gladiator frog, Hypsiboas faber, to components and/or dissolution products of fertilizers varies predictably through ontogeny by sequentially exposing eggs, embryos, and larvae to ammonium nitrate, sodium nitrate, sodium nitrite, and ammonium sulfate. Nitrate was the least toxic nitrogen ion regardless of stage; the most deadly compound was ammonium or nitrite, depending on stage. Overall, embryos were more sensitive to inorganic nitrogen than more advanced developmental stages, indicating that the jelly capsule envelopes that surround the egg do not provide effective protection against contaminants. However, for most compounds tested, the relationship between lethal concentrations (LCx), no-observed effect concentrations (NOEC), and lowest observed effect concentrations (LOEC) and developmental stage or mass was not monotonic. Whereas for sodium nitrate sensitivity declined asymptotically with developmental stage, for ammonium nitrate, sodium nitrite, and ammonium sulfate, sensitivity declined through early development and then increased again at Gosner stage 25. Together with previously published literature, this finding indicates no single and predictable trend in sensitivity through development, even if we restrict our analysis to a relatively narrow range of organisms and contaminants. Such a relationship creates complex scenarios of risk as a function of the phenology of application of fertilizers and of the temporal variation in environmental factors that modulate nitrogen speciation and toxicity in and near agricultural fields.

Partitioning the turnover and nestedness components of beta diversity: Partitioning beta diversity

Article

Oct 2009
GLOBAL ECOL BIOGEOGR

Andrés Baselga

A protocol for data exploration to avoid common statistical problems. Methods Ecol

Article

Jan 2010

Land clearing and the biofuel carbon debt

Article

Jan 2007

MuMIn: Multi-model inference

Code

Jan 2013

Kamil Bartoń

Tools for performing model selection and model averaging. Automated model selection through subsetting the maximum model, with optional constraints for model inclusion. Model parameter and prediction averaging based on model weights derived from information criteria (AICc and alike) or custom model weighting schemes. [Please do not request the full text - it is an R package. The up-to-date manual is available from CRAN].

Mixed Effects Models and Extensions in Ecology With R

Book

Jan 2009

Team RDC.R: A Language And Environment For Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria

Technical Report

Jan 2012

Core R Team

Mixed Effect Models and Extensions in Ecology With R

Book

Jan 2009

Limitations of linear regression applied on ecological data. - Things are not always linear additive modelling. - Dealing with hetergeneity. - Mixed modelling for nested data. - Violation of independence - temporal data. - Violation of independence spatial data. - Generalised linear modelling and generalised additive modelling. - Generalised estimation equations. - GLMM and GAMM. - Estimating trends for Antarctic birds in relation to climate change. - Large-scale impacts of land-use change in a Scottish farming catchment. - Negative binomial GAM and GAMM to analyse amphibian road killings. - Additive mixed modelling applied on deep-sea plagic bioluminescent organisms. - Additive mixed modelling applied on phyoplankton time series data. - Mixed modelling applied on American Fouldbrood affecting honey bees larvae. - Three-way nested data for age determination techniques applied to small cetaceans. - GLMM applied on the spatial distribution of koalas in a fragmented landscape. - GEE and GLMM applied on binomial Badger activity data.

Metacom: An R package for the analysis of metacommunity structure

Article

Apr 2014
ECOGRAPHY

Tad Dallas

Metacommunity theory is an extension of metapopulation theory with the goal of understanding how ecological communities vary through space and time. One off-shoot of metacommunity theory deals with understanding how community structure varies along biotic or environmental gradients. The Elements of Metacommunity Structure framework is a three-tiered analysis of metacommunity structure that enables the user to identify metacommunity properties that arise in site-by-species incidence matrices. These properties can then be related to underlying variables that influence species distributions. The EMS framework is now implemented in metacom, an open source R package that allows for the analysis and plotting of metacommunities.

Consequences of agroindustrial sugarcane production to freshwater biodiversity

Abstract and Figures

Supplementary resource (1)

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