Boletín de la Sociedad Zoológica del Uruguay, 2024

Vol. 33 (2): e33.2.5

ISSN 2393-6940

https://journal.szu.org.uy

DOI: https://doi.org/10.26462/33.2.5

ABSTRACT

Oil palm cultivation and the conversion of tropical forests

to pastures are impacting freshwater tropical systems.

This study examines periphyton biomass, richness,

diversity, and community composition in streams affected

by forests, pastures, and oil palm plantations, with and

without forest buffer strips. Streams shaded by forests or

riparian buffers exhibited more canopy cover, lower water

temperatures, and reduced light, while those in pastures

and unbuffered plantations had higher periphyton

biomass, indicated by elevated chlorophyll-a levels.

Periphyton richness and diversity were higher in pasture

streams compared to forested ones and streams through

oil palm areas. Common periphyton taxa differed among

stream depending of land cover. Streams in buffered and

unbuffered palm plantations featured taxa such as

Navicula and Gyrosigma, whereas pasture streams

commonly included were characterized by genera such as

Cymbella, and Gonatozygon, and forest stream

communities featured Phormidium and Eunotia. Pasture

streams displayed altered taxa richness and diversity

compared to the other land uses. There were no

significant differences in periphyton communities between

the two oil palm cultivation types, indicating that

conservation buffers may not effectively protect

periphyton communities in these settings. This research

highlights the need for further studies on the impacts of

agricultural practices on aquatic primary producers.

Keywords: benthic algae, land cover change, pasture,

palm oil.

RESUMEN

La influencia de la cobertura del suelo en las

comunidades de periphyton en arroyos del norte de

Guatemala. La conversión de bosques tropicales por

palma aceitera y potreros impactan en las comunidades

acuáticas. Estudiamos los cambios en la riqueza,

diversidad y comunidades de perifiton en arroyos de

bosques, potreros y plantaciones de palma aceitera, con y

sin franjas ribereñas. Los arroyos en bosques o

plantaciones con franjas ribereñas mostraron mayor

cobertura de dosel, bajas temperaturas de agua y menor

entrada de luz que los arroyos en potreros y plantaciones

sin franjas ribereñas. Estos últimos presentaron mayor

biomasa de perifiton, evidenciada por altos niveles de

clorofila-a. La riqueza de taxa y diversidad fueron

significativamente mayores en arroyos de potreros en

comparación con los de bosque y palma aceitera. En los

arroyos de plantaciones de palma predominaban taxones

como Navicula y Gyrosigma. En los de potreros Cymbella

y Gonatozygon, y en los de bosque, Phormidium y

Eunotia. No se encontraron diferencias significativas en

las comunidades de perifiton entre los dos tipos de cultivo

de palma aceitera, lo que indica que las franjas de

conservación pueden no proteger eficazmente a las

comunidades de perifiton en estos entornos. Destacamos

la necesidad de realizar más estudios sobre los impactos

de las prácticas agrícolas en los productores primarios

acuáticos.

Palabras clave: algas bentónicas, cambio de

cobertura terrestre, pastos, aceite de palma

INTRODUCTION

Tropical forests provide essential ecosystem

services and are home to more than half of the species

on earth (Myers, 1988). Despite their importance,

tropical forests have been rapidly declining due to

deforestation caused by agricultural expansion (Giam,

2017; Laurance et al., 2014) and pasture lands

Bol. Soc. Zool. Uruguay (2ª época). 2024. ISSN 2393-6940Vol. 33 (2): e33.2.5

THE INFLUENCE OF LAND COVER ON PERIPHYTON COMMUNITIES IN STREAMS IN

NORTHERN GUATEMALA

1,2, 1,3 4 4

Natalia Vargas-López Krista A. Capps Dean Jacobsen Oscar A. Rojas-Castillo

1Odum School of Ecology, University of Georgia, USA

2Centro de Estudios de Atitlán, Universidad del Valle de Guatemala, Sololá, Guatemala

3River Basin Center, University of Georgia, USA

4Freshwater Biology Section, Department of Biology, University of Copenhagen, Denmark

Correspondence author: navargalo@gmail.com

Fecha de recepción: 13 de junio de 2024

Fecha de aceptación: 25 de noviembre de 2024

, , , .

VARGAS-LOPEZ et al.

(Kaimowitz, 1996). Oil palm cultivation (Elaeis

guineensis Jacq.) is a primary driver of deforestation in

the tropics and is the fastest-expanding crop in the

world (Davis et al., 2020; Vijay et al., 2016). In Latin

America, pastureland has also significantly replaced

tropical forests, making it one of the most prominent

changes in land cover (Graesser et al., 2015;

Wassenaar et al., 2007). Pasture and palm cultivation

homogenizes habitats, driving the loss of biodiversity

(Meijaard et al., 2018; Reiners et al., 1994) with

negative impacts documented for insects (Fitzherbert

et al., 2008; Kruess & Tscharntke, 2002).

Oil palm cultivation and pastures can also

significantly impact aquatic ecosystem function and

aquatic biodiversity particularly through the

modification of riparian vegetation (Rojas-Castillo et

al., 2024a). Riparian vegetation plays a crucial role as a

buffer to streams subject to land cover conversion,

mitigating the adverse effects of changes in the

surrounding environment on aquatic ecosystems

(Naiman & Décamps, 1997; Reichenberger et al.,

2007). Land conversion in the riparian zone can affect

in-stream sedimentation rates (Koren & Klein, 2000),

water quality parameters such as dissolved oxygen,

temperature, and nutrients (Chellaiah & Yule, 2018),

and the availability of allochthonous food sources and

microhabitats in streams (Gonçalves et al., 2014).

When riparian buffers are completely removed, intense

light can penetrate streams (Osborne & Kovacic,

1993), and surface runoff can enter streams carrying

high concentrations of nutrients (Kennedy, 1984;

Kuriata-Potasznik et al., 2020). Research has shown

that the conversion of land to oil palm cultivation can

significantly alter macroinvertebrate (Luiza-Andrade et

al., 2017), and fish communities (Chua et al., 2020).

Conversion to pasture can influence leaf litter

decomposition (Lemes da Silva et al., 2020) and

ambient nutrient concentrations (Neill et al., 2001).

Relatively little work has focused on photosynthetic

microorganisms such as periphyton in oil palm

plantation streams (Rojas-Castillo et al., 2024a).

Though some work has considered the impact of

conversion to pasture on periphyton communities,

there is still much to be learned (Tromboni et al., 2019).

Periphyton communities are essential components

of stream ecosystems, supporting food webs (Wu,

2017) and biogeochemical cycling (Hagerthey et al.,

2011). Periphyton communities, found abundantly in

various stream ecosystems, exhibit remarkable

diversity and demonstrate swift adaptability to shifts in

water quality (Li et al., 2010). They respond to changes

induced by shifts in land cover and environmental

conditions, manifesting alterations in both their

structural composition and functional dynamics. For

instance, streams draining pasture, or agriculture (e.g.,

coffee plantations), have shown greater taxon richness

and diversity compared to forested streams (Vázquez

et al., 2011). Additionally, increases in algal biomass

are common when land conversion opens the canopy,

allowing more light, and potentially more nutrients, to

enter streams (Quinn et al., 1997; Von Schiller et al.,

2007; Tromboni et al., 2019). The traits of community

members can also shift in response to land conversion,

moving towards communities dominated by tolerant

taxa (Bere & Tundisi, 2011; Mangadze et al., 2015;

Tromboni et al., 2019). Collectively, the patterns

suggest that periphyton communities may be a

valuable, but underutilized bioindicator for monitoring

changes in streams impacted oil palm plantations,

providing deeper insights into the agricultural impacts

on aquatic ecosystems.

Our study was conducted in Guatemala, the sixth

major oil palm producer in the world (IndexMundi,

2024), which has also experienced a significant

increase in land allocated to pasture in recent years

(Carr, 2004). Conversion to pasture land and oil palm

cultivation are interconnected, as the expansion of oil

palm plantations in the country has primarily occurred

at the expense of pastures, in addition to land

conversion from other crops and forests (Furumo &

Aide, 2017). To evaluate the effects of land-cover

change and the expansion of the oil palm monocrops

on periphyton communities in Guatemalan streams,

we conducted a comparison of periphyton

communities in streams draining pastures, forests, and

two types of oil palm plantations -those that implement

riparian buffers as a mitigation strategy and those that

do not. We aim to answer (i) how does land use relate to

stream algae biomass (measured as benthic

chlorophyll-a concentrations)? and, (ii) what are the

impacts of land-use change on periphyton richness,

evenness, and community composition? We expect

that streams with high canopy cover (forest and oil

palm with buffer strips) would have reduced algae

biomass, species richness and diversity compared to

open canopy streams (pasture and unbuffered oil palm

streams) due to light limitation and lower temperatures.

Additionally, we expected that the community

composition in open canopy streams would be

characterized by taxa associated with greater light

input, temperature, nutrients, and turbidity compared to

the closed canopy streams, as riparian vegetation is

also expected to reduce nutrient and sediment runoff.

METHODS

Study site and experimental design

We worked in the Lachuá Ecoregion of northern

Guatemala, which is a low-lying, karst- dominated

landscape. The average temperature is 25.3°C, and

annual precipitation in the region is greater than 2500

mm with two seasons predominating: dry (February to

May) and rainy (June to October) (CONAP, 2003). The

ecoregion comprises the Laguna Lachuá National Park

Bol. Soc. Zool. Uruguay (2ª época). 2024. ISSN 2393-6940Vol. 33 (2): e33.2.5

3The influence of land cover on periphyton communities in streams in northern Guatemala

(LLNP), declared a RAMSAR site of international

importance for wetland conservation (RAMSAR,

2004). It is also considered one of Guatemala's last

remnants of tropical rainforests composed of dense

vegetation of at least 76 plant families (CONAP, 2003).

Surrounding the LLNP, land cover is mixed.

Approximately 55% of the forest cover has been

replaced by pastures, human settlements, roads, and

annual crops (Quezada et al., 2014). Agriculture

practices consist of subsistence crop production, such

as corn, beans, and chili, and also included larger

plantations of cardamom, coffee, cocoa, rubber, and oil

palm (MAGA, 2012; Quezada et al., 2014). Oil palm

cultivation in the Lachuá Ecoregion began in 2006

(MAGA, 2012), and often involved deforestation or the

replacement of previously intervened lands, primarily

pastures (Furumo & Aide, 2017), and currently

northern Guatemala has the largest area of oil palm

plantations in the country (GREPALMA, 2019). The

study was conducted during the rainy season between

July and August of 2021 when nutrient and sediment

runoff was expected to be greater. We collected

samples in 19, first and second-order streams draining

tropical forest (FO; n = 7), pasture (PA; n = 6), and oil

palm plantations with riparian buffers (OPB; n = 3) and

without riparian buffers (OP; n = 3) (Fig. 1).

Catchment and stream characteristics

We measured land cover, water temperature and

light input, and water quality variables in all study

streams. To estimate land cover, we employed the

stream catchment areas previously delimited by Rojas-

Castillo et al., (2023). The percentage of each land

cover (i.e., tropical forest, palm oil, pasture, secondary

vegetation or roads) was estimated using Google Earth

2021 satellite images (Google Earth engine, 2021) by

manually delimiting polygons and then transforming

into shape files in QGis (QGIS Development Team,

2019) to calculate the area (m ) of each type of land

cover. The estimation of the canopy cover density was

obtained from Rojas-Castillo et al. (2023).

Water temperature and light input were measured

using HOBO® Pendant MX Temp/Light data loggers in

each stream. The loggers were programmed to

measure temperature (°C) and light (lux) every 30

minutes over a month. Physico-chemical parameters

were measured once during the sampling period, i.e.,

one deployment of the probes and one water sample

that was collected during the study. Variables

measured included dissolved oxygen (DO mg/L),

conductivity (µS/cm), turbidity (NTU), and pH, that

were measured using a multiparametric probe (Model

6000; YSI, Yellow Springs, OH, USA), pH-meter

(ecoTestr pH2) and turbidimeter (Eutech-100). We also

collected and analyzed samples for Biochemical

Oxygen Demand (DBO; mg/L), NO (mg/L), NH (mg/L),

3 4

inorganic nitrogen, SiO (mg/L), and PO (mg/L) using a

2 4

single, 2-liter water sample from each stream using

acid-washed plastic jars. Samples were refrigerated

until analysis in the Analytical Solutions laboratory

Chemical (SiO only) and the Environmental Research

Laboratory (LIQA; the rest of the analytes).

Periphyton biomass: benthic chlorophyll-a

concentrations 2

The concentration of benthic chlorophyll-a (mg/m ),

a proxy for algal biomass, was measured on stones

and in sediment following Jacobsen et al. (2016).

Replicate samples were collected at four points in the

streams, at least 20 m apart. The total number of

replicates collected was: FO = 28; PA = 24; OP = 12;

OPB = 12. Each replicate consisted of the collection of

3 stones and 3 core sediments. Stones were collected

manually, and cores were obtained from the superficial

layer of sediments using a 55-cc syringe. The samples

were placed in bottles with 96% ethanol (Pápista &

Böddi, 2002) and stored in the dark in a refrigerator for

48 hours until the chlorophyll was extracted. To

complete the extraction, the ethanol from samples was

filtered by gravity with Whatman® glass microfiber

filters, grade GF/F, 0.7 μm pore. The solvent obtained

was stored in aluminum-lined bottles under

refrigeration for 24 hours. The solvent was processed

in HACH DR 6000 spectrophotometer at 665 nm and

750 nm. Once we obtained the values from the

spectrophotometer, we calculated the surface area of

the sediments and rocks. The sediment's surface area

was equivalent to the diameter of the syringe (seven

cm ), and the rock surface area was obtained from the

formula of Jacobsen et al. (2016) that includes the

measurement of the length, width and height of the

stones. The benthic chlorophyll-a concentration was

quantified spectrophotometrically by the method

described by Søndergaard & Riemann (1979) using

the specific coefficient of absorption of chlorophyll in

ethanol (Jacobsen et al., 2016).

Periphyton communities

To evaluate periphyton community composition, we

collected periphyton from three locations (0m, 50m,

and 100m) in each stream reach (Rojas et al., 2022).

The total number of replicates collected from each

habitat type was: FO = 21; PA = 18; OP = 9; OPB = 9.

Substrates were not distributed evenly among

streams, so in pasture and oil palm streams, we

collected on rocks, when possible, but we also

collected samples from wood when rocks were not

available. To delineate the sample area on the hard

surfaces, we used a four-centimeter diameter PVC

ring, and gently scraped from the surface using a

brush. We washed the scraped material with stream

water and fixed in 4% lugol (Stevenson & Bahls, 1999).

Samples were stored in dark bottles until they were

analyzed in the laboratory. The initial sample volume of

100 mL underwent 24-hour sedimentation, followed by

volume reduction to 50 mL through vacuum filtration.

Bol. Soc. Zool. Uruguay (2ª época). 2024. ISSN 2393-6940Vol. 33 (2): e33.2.5

VARGAS-LOPEZ et al.

Subsequently, it underwent an additional 24-hour

sedimentation, resulting in a further reduction in

volume to 18 mL (Bellinger & Sigee, 2010). We

conducted the volume reduction process at room

temperature, on a horizontal surface and out of direct

sunlight in order to be able to identify and quantify

organisms in a smaller volume (20 mL) than the initial

one (100 mL) (Karlson et al., 2010).

We identified the soft algae and diatoms in wet

mounts to the genus or morphospecies level using a

Labomed Lx400 Phase Contrast Microscope. The

same taxonomic resolution was used to estimate taxa

richness and the community composition in each

sample by counting the first 200 organisms in each

sample (Stevenson & Smol, 2015). We used keys of E.

Bellinger & Sigee (2015); Bicudo & Menezes (2006);

Cox (1996); Prescott (1978); Wehr & Sheath (2003).

After completing the identification process, we

preserved the samples in 2 mL of 10% formalin to

ensure they remain intact for an extended period

(Karlson et al. 2010). An adaptation of the Arriola et al.

(2015) and Biggs & Kilroy (2000) formulas were used to

obtain the relative density estimate for each sample

(formula 1).

Formula 1 -1

Organisms density cm = (Counted organisms x Volf)

/ (Voli x Volc) / (Diameter)

Where,

Counted organisms: total number of organisms

counted in each sample.

Volf: concentrated volume (18 mL).

Volfi: collected volume (100 mL).

Volfc: volume counted to reach 200 organisms.

Diameter: Sampling diameter, according to PVC ring

(4 cm x 5 substrates = 20 cm).

Statistical analysis

To assess whether differences in water chemistry

could be documented among land cover types, we

used PERMANOVA, followed by Pairwise-Permanova

when needed (Table 1) (Gentleman et al., 2008). Using

the raw data from the periphyton counts, we calculated

the observed and expected species richness (S), and

Simpson index (D) with the iNEXT package in R using

the ChaoRichness, and ChaoSimpson with 95%

confidence intervals (Hsieh et al., 2016). For obtaining

Pielou Evenness (J) we used the formula J = Shannon-

Weiner/log(Richness) (Alatalo, 1981). For our

Bol. Soc. Zool. Uruguay (2ª época). 2024. ISSN 2393-6940Vol. 33 (2): e33.2.5

Fig. 1. Maps of the catchment area of each stream and their predominant land cover. (A) the location of the Lachuá

Ecoregion in Guatemala, (B) the general location of the catchment areas, (C-E) dominant land cover in each catchment

(Google Earth engine, 2021).

5The influence of land cover on periphyton communities in streams in northern Guatemala

subsequent analyses, we used the Expected Richness

and Expected Simpson values derived from the iNEXT

package, as these indices (S and D) tend to be

sensitive to undetected presence of rare species and

the impact of sampling effort (Colwell et al., 2012). To

estimate the effect of land use on S, D, J, and

chlorophyll-a concentration, we conducted analysis of

variance (ANOVAs) on linear mixed-effect models, with

stream as a random effect (Bates et al., 2015). In cases

when land cover significantly impacted a response

variable, we also ran a post hoc Tukey-Kramer test to

evaluate differences among treatments (Herberich et

al. (2010);Code in supplementary material as

01Biodiversity and 03Chlorophyll).

We ran a non-metric multidimensional scaling

(NMDS) with the Bray-Curtis Index using the

periphyton density to evaluate differences in commu-

nity structure for each stream (Code in supplementary

material as: 04Community). To test the relative influ-

ence of the environmental variables on periphyton

communities, we used the function envfit from the

vegan package (Gentleman et al., 2008). We then

completed a PERMANOVA and a pairwise

PERMANOVA to compare differences in the observed

group in the NMDS (Anderson, 2017). To identify the

representative taxa from each of the groups identified

through NMDS, we performed an indicator species

analysis using the multipatt function from the

indicspecies R package (De Cáceres & Legendre,

2009). Since buffered and unbuffered streams in oil

palm were not statistically different (PairwisePerma-

nova; r 0.237, p = 0.400), we used only three groups in

the indicator species analysis: forest, pasture, and oil

palm.

RESULTS

Land cover and physicochemical parameters

The study catchments had at least 70% of their area

covered by the designated land cover, i.e., forest, oil

palm plantation or pasture (Table 1). All forest

catchments on Laguna Lachuá National Park were

characterized by 100% forest cover. In contrast,

pasture catchments had more variability, but pasture

cover in all watersheds exceeded 72%. The

catchments dominated by oil palm (OP1-OP3) were

covered by 96% palm cover, while the other palm sites

(OP4-OP6) had 71% palm cover and 21% secondary

vegetation.

Of the parameters measured, light, temperature,

dissolved oxygen, and turbidity were significantly differ-

ent among land cover treatments. Light input was sig-

nificantly higher in pasture and unbuffered oil palm

(PERMANOA p = 0.001). In pasture streams, the tem-

perature was almost 4°C higher (PERMANOA p =

0.001) and dissolved oxygen was almost 3 mg/L lower

compared to streams in all other land cover

(PERMANOA p = 0.002). Palm oil streams with and

without a buffer strip had the highest turbidity compared

to forest and pasture streams (PERMANOA p = 0.001).

Relative to pasture and forest streams, oil palm

streams with no buffer had two times and four times

water turbidity, and oil palms streams with buffers had

three times and seven times greater turbidity, respec-

tively (Table 2). Phosphorus (PO ) concentrations were

below detection in all study streams and nitrogen forms

(NO PERMANOA p = 0.157; NH PERMANOVA p =

3 4

0.156; and inorganic N (PERMANOA p = 0.163) and

SiO (PERMANOA p = 0.233) did not show a statistical

difference.

Benthic chlorophyll-a2

Chlorophyll-a in sediment samples (mg/m ) was

significantly impacted by land cover (ANOVA; F =

5.64879, p = 0.0085; Fig 2). The greatest concentra-

tions were in unbuffered oil palm streams (mean= 10.5,

sd = 10.3), followed by pasture (mean = 9.9, sd = 8.6),

buffered oil palm (mean = 1.3, sd = 0.8) and forest

(mean = 1.1, sd = 0.7). Post hoc tests revealed the

strongest differences in the comparison of pasture with

forest and buffered oil palm streams and with

unbuffered oil palm and forest (Fig. 2. Supplementary

material 1). Though there was variation among treat-

ments in benthic chlorophyll estimates collected from

stones (mg/m ), the difference was not statistically

significant (ANOVA; F = 3.090275, p = 0.059; Fig. 2).

Despite no significant difference was shown by the test,

the stones exhibited a comparable pattern to sediment

samples: greatest concentrations in pasture (mean =

Bol. Soc. Zool. Uruguay (2ª época). 2024. ISSN 2393-6940Vol. 33 (2): e33.2.5

Table 1. Catchment and canopy cover showing mean and standard deviation in parenthesis of each land use (FO = Forest, OPB = Oil

Palm with riparian buffer, PA = Pasture, OP = Oil Palm).

Land cover Land cover Canopy cover (%)

Forest (%) Pasture (%) Oil palm (%) Secondary vegetation (%) Roads (%) Rojas-Castillo et al., (2023)

FO 100 (0) 0 (0) 0 (0) 0 (0) 0 (0) 83 (2.5)

OPB 0 (0) 0 (0) 71 (30.3) 27 (32.1) 2 (2.1) 81 (0.9)

PA 5 (12.9) 72 (28.9) 3 (6.3) 18 (12.9) 0.33 (0.5) 14 (17.5)

OP 0 (0) 0 (0) 96 (1) 1 (2.3) 2 (1.5) 37 (12.3)

VARGAS-LOPEZ et al.

15.9, sd = 18.6), followed by unbuffered oil palm (mean

= 9.2, sd = 8.3), forest (mean = 5.9, sd = 9.1), and buf-

fered oil palm (mean = 0.9, sd = 1.2).

Periphyton diversity and community composition.

Collectively, among all of our sites, we documented

a total of 69 taxa belonging to 42 genera, distributed in

5 phyla: 36% Bacillariophyta, 29% Charophyta, 17%

Cyanophyta, 14% Chlorophyta, and 5% Rhodophyta

(Supplementary material 2). Overall, we found greater

taxa richness and diversity in pasture streams relative

to the other land uses. Total taxa richness (Fig. 3)

ranged from 11 to 34 and was significantly impacted by

land cover (ANOVA; F = 5.7869, p = 0.0078). Taxa

richness was higher in pasture (mean = 24.0; sd = 5.7)

followed by unbuffered oil palm (mean = 19.1; sd = 6.0),

buffered oil palm (mean = 17.7; sd = 4.5) and forest

(mean = 17.4; sd = 3.4) streams. Post hoc Tukey test

indicated that streams in pastures had the highest taxa

richness compared to forest streams (Tukey, p <0.001)

and oil palm with buffer strips (Tukey; p = 0.0174).

Richness did not vary between buffered and

unbuffered oil palm (Tukey: p = 0.9447; Supplementary

material 3) and there was no significant difference

between streams in either type of oil palm plantations

and forest streams (Tukey for OP: p = 0.8551 and OPB:

p = 0.9990; Supplementary material 3).

Diversity, measured with Simpson Index ranged

from 0.507 to 0.942 and was also significantly

influenced by land cover (ANOVA; F = 3.491, p =

0.0423; Fig. 3). The lowest diversity was found in

unbuffered (mean = 0.81; sd = 0.04) and buffered oil

palm streams (mean = 0.82; sd = 0.12). The highest

diversity was found in pasture (mean = 0.89; sd = 0.03)

and forest streams (mean = 0.86; sd = 0.06). Post hoc

Tukey test indicated that diversity in pasture streams

was significantly higher compared to unbuffered oil

palm streams (Tukey; p = 0.0317). There was also a

marginal relationship between pasture streams and

buffered oil palm (Tukey; p = 0.0537). Diversity did not

vary between buffered and unbuffered oil palm (Tukey:

p = 0.9983) or between forested systems and either

type of oil palm plantation (Tukey for OP: p = 0.3788

and OPB: p = 0.4999; Supplementary material 4).

Pielou Evenness Index ranged from 0.444 to 0.942;

however, it was not significantly influenced by land

cover (ANOVA; F = 1.812, p = 0.1883).

The periphyton community composition was

impacted by land cover (Permanova; F = 4.6856, p =

0.001). Pairwise Permanova showed that forest

streams differed from pasture (p = 0.009) and buffered

and unbuffered oil palm streams (p = 0.006). Pasture

streams also differed from the buffered and unbuffered

oil palm streams (p = 0.009; Fig. 4). The nonmetric

multidimensional scaling (NMDS; stress value =

0.166921) showed that the periphyton community

composition in forest streams was influenced by

canopy coverage (R 0.7518, p = 0.001) and dissolved

oxygen (R 0.4132, p-value 0.028). In the pasture

streams the variables that showed a significant

influence were light (R 0.7024, p = 0.002), water

2 2

temperature (R 0.6119, p = 0.004), and NO (R

Bol. Soc. Zool. Uruguay (2ª época). 2024. ISSN 2393-6940Vol. 33 (2): e33.2.5

Table 2. Stream environmental characteristics, showing mean and standard deviation in parenthesis of each land use (FO = Forest,

OPB = Oil Palm with riparian buffer, PA = Pasture, OP = Oil Palm). Variables with significant statistical difference (PERMANOVA) in bold

and with the p value in parentheses. Post hoc test (Pairwise PERMANOVA) differences are shown with letters, e.g., A, B, C, AB. All PO

concentrations were no detectable (ND).

Land cover Nutrients

SiO (mg/L) Inorganic Nitrogen (mg/L) NH (mg/L) NO (mg/L) PO (mg/L)

2 4 3 4

PERMANOVA p = 0.199 p = 0.163 p = 0.146 p = 0.051

FO 14.37 (5.6) 0.05 (0.04) 0.04 (0.04) 0.01 (0.0) ND

OPB 9.23 (1.3) 0.06 (0.08) 0.06 (0.08) 0.00 (0.0) ND

PA 13.67 (3. 8) 0.08 (0.03) 0.05 (0.02) 0.03 (0.03) ND

OP 10 (2.9) 0.09 (0.05) 0.07 (0.04) 0.03 (0.01) ND

Land cover Physicochemical variables

Light (lux) Temperature (°C) DO (mg/L) Turbidity (ntu) Conductivity pH

PERMANOVA p = 0.001 p = 0.001 p = 0.002 p = 0.001 p = 0.097 p = 0.137

FO 74.6 (49.8) A 24.7 (0.4) A 5.4 (1.6) A 6.7 (4.1) A 52.8 (26.1) 6.7 (0.3)

OPB 5.2 (4.8) AB 24.6 (0.5) A 5.1 (0.9) A 47.3 (27.4) B 98.6 (29.3) 6.7 (0.2)

PA 991.8 (269.3) C 28.4 (1.5) B 1.8 (0.4) B 14.1 (6.9) A 106.4 (50.5) 6.9 (0.2)

OP 778.9 (864.9) BC 24.7 (1.4) A 5.2 (1.1) A 28.7 (4.5) AB 68.1 (29.5) 6.6 (0.4)

0.4518, p = 0.008). For the oil palm streams with and

without a riparian buffer strip, turbidity (R 0.4687, p =

0.012) seemed to be the variable influencing the

community composition (Fig. 4). The indicator species

analysis showed that from the 69 taxa reported, 29 can

describe communities in the different land cover (Table

3). 18 taxa were associated with pasture streams, 6

taxa were associated with forest streams, and 5 were

taxa associated with oil palm streams with and without

a riparian buffer strip.

DISCUSSION

This study demonstrated that land conversion influ-

ences algal biomass, periphyton taxa richness, and

diversity compared to streams flowing through forested

landscapes in Guatemalan streams. Specifically, we

found significant differences in the structure and com-

position of periphyton in streams draining pasturelands

relative to the other streams in our study. We found that

benthic algal biomass was greater in landscapes domi-

nated by that remove riparian buffers, such as pastures

but also oil palm plantations without buffers. We found

no significant differences in taxa richness and diversity

between forested streams and those in oil palm planta-

tions. Similarly, there was no distinction in richness and

diversity between palm streams with riparian buffers

and those without. Yet, periphyton community compo-

sition was impacted by dominant land cover, and com-

munities collected in streams impacted by oil palm

cultivation were similar, containing more tolerant spe-

cies, in buffered and unbuffered systems. Our results

illustrate that land cover change can influence

photosynthetic microorganisms, as previous studies

show for before (Bere & Tundisi, 2011; Burgos-

Caraballo et al., 2014; Quinn et al., 1997; Tromboni et

al., 2019; Vázquez et al., 2011; Von Schiller et al.,

2007). Notably, we anticipated differences between

forest streams and oil palm plantations; however, our

findings did not support this prediction. We also

expected to find a difference between periphyton in oil

palm with and without a buffer strip because of

differences in riparian shading, contribution to

allochthonous material inputs. However, the

differences we documented were minimal.

Benthic chlorophyll-a and periphyton richness

and diversity.

Regardless of the dominant land cover, all streams

in this study were classified as oligotrophic-

mesotrophic based on chlorophyll concentrations

Bol. Soc. Zool. Uruguay (2ª época). 2024. ISSN 2393-6940Vol. 33 (2): e33.2.5

The influence of land cover on periphyton communities in streams in northern Guatemala

Fig. 2. Box plot of repeated measures of Chlorophyll-a mg/m concentrations collected from sediment (left) and stone (right)

among streams flowing through different land cover treatments (forested (FO), oil palm (OP), oil palm with buffer (OPB), and

pasture (PA)).

-2 -2

(mean 20 mg m and maximum limit 60 mg m ; Dodds

et al., 1998). However, pasture streams were where we

observed the most significant differences in periphytic

algae, including biomass, taxa richness, and diversity.

This may have been attributed to increased light pene-

tration in pasture streams, as taxon richness, diversity

and benthic chlorophyll-a concentrations can be influ-

enced by light (Quinn et al., 1997; Vázquez et al., 2011;

Von Schiller et al., 2007; Tromboni et al., 2019). Buffer

strips reduce the amount of light entering streams

(Montgomery & Chazdon, 2001), consequently limiting

the growth and reproduction of algae (Hill, 1996). In our

systems, closed canopy streams (forest and oil palm

with riparian buffer) had five times more canopy cover

than pasture streams, and two times more canopy than

oil palm streams without a riparian buffer (Rojas-

Castillo et al., 2023).

We initially expected that streams associated with

unbuffered oil palm plantations would exhibit similar

conditions to those in pasture areas, as we predicted

that both types of land conversion would similarly affect

light penetration and nutrient inputs. However, our

results did not support this prediction. To assess the

shading effect of vegetation in the riparian zone, we

measured the percentage of canopy cover. However,

this metric did not account for the presence of shrubs or

grasses along the stream edges within oil palm

plantations, which can limit light entry. Similar

observations have been reported in other plantation

studies (Chellaiah & Yule, 2018; Lucey et al., 2018).

Additionally, the shade produced by the oil palms

themselves may have influenced our results. Oil palms

can grow up to 30 meters in height (Arias et al., 2009),

and their canopies may have restricted the amount of

light reaching the streams.

Ambient nutrient concentrations can also be

impacted by land cover change within a watershed,

and access to nitrogen or phosphorus can influence

algal abundance (Mangadze et al., 2015; Tromboni et

al., 2019) and biofilm diversity (Burgos-Caraballo et al.,

2014). Nutrients can also interact with light to support

greater biomass (Pacheco et al., 2022). Nutrient data in

this study were exceptionally limited (i.e., one sample

per stream reach); therefore, drawing conclusions

about predicted changes in water chemistry and

subsequent interactions with the periphyton

community should be done with care. We did not

document any statistically significant difference

between N or P and predominant land cover in our

study. However, this again could be due to extremely

low P concentrations (all below the limit of detection)

and the small number of samples we collected. Future

work should examine interactions between nutrients

and light in streams impacted by palm cultivation.

Turbidity in oil palm streams may have also influ-

enced periphyton communities through light occlusion

(Mori et al., 2018). Our data indicated that buffered and

unbuffered oil palm streams had the highest water

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VARGAS-LOPEZ et al.

Fig. 3. Average of the A) Estimated Richness (S), and B) Estimated Simpson (D) for each land cover treatment (forested (FO), oil

palm (OP), oil palm with buffer (OPB), and pasture (PA)). Bars represent standard error.

turbidity. Oil palm plantations can have greater water

turbidity due to soil erosion (Comte et al., 2012; Sahat

et al., 2016; Afandi et al., 2017) and this could have

important effects from a button-up perspective. For

instance, Chua et al., (2020) hypothesized that due to

high turbidity, oil palm streams could have reduced

autochthonous primary production and therefore result

in changes in fish traits. This may be especially impor-

tant for secondary consumers in unbuffered palm plan-

tations because they receive less allochthonous mate-

rial (Chua et al., 2020; Rojas-Castillo et al., 2023) and

therefore there will be fewer food resources (Brett et al.,

2017). The implementation of riparian buffers in oil

palm plantations aimed to soil erosion might need to be

improved in the plantation under study (Lucey et.al.,

2018). Streams adjacent to oil palm plantations lacking

buffer strips are directly affected by agricultural activi-

ties, allowing sediments to enter the water, and conse-

quently elevating turbidity levels (Mercer et al., 2014;

Luiza-Andrade et al., 2017).

Periphyton community composition

The periphyton communities we documented

through this study grouped by the type of dominant land

cover in the watershed. In forested streams, some of

the taxa we documented, including diatoms such

Eunotia sp. and Frustulia sp. are indicators of

oligotrophic systems that are typically rich in oxygen,

and poor in inorganic nitrogen inputs (Schneider et al.,

2013; Van Dam et al., 1994). In Brazil, some Eunotia

species, were reported in streams with high forest

cover and low levels of BOD5 (Bere & Tundisi, 2011).

Our work supports studies conducted in Mexican

streams by Ramírez-Babativa & Vázquez, (2015) and

Vázquez et al., (2011) who documented species of

Frustulia in well-conserved forested streams in Mexico.

In forested systems we also documented Cyanophyta

taxa inhabiting forest streams, Stigonema sp. and

Phormidium sp. Cyanobacteria can thrive in forest-

associated streams due to the phycobilin complex

capacity to utilize long wavelengths, enabling their

Bol. Soc. Zool. Uruguay (2ª época). 2024. ISSN 2393-6940Vol. 33 (2): e33.2.5

The influence of land cover on periphyton communities in streams in northern Guatemala

Table 3. Indicator taxa derived using the multipatt function in R. P-values are in parentheses.

Land cover Indicator species

Forest (7 taxa) Bacillariophyta Cyanophyta

Eunotia sp 3 (0.008) Phormidium sp 1 (0.009)

Frustulia sp 1 (0.011) Stigonema sp 1 (0.0013)

Amphipleura sp 1 (0.043) Chlorophyta

Morpho genera 1 (0.025)

Pasture (16 taxa) Bacillariophyta Charophyta

Stauroneis sp 1 (0.003) Closterium sp 1 (0.001) sp 2 (0.001) sp 3 (0.043)

Gomphonema sp 1 (0.002) Cosmarium sp 2 (0.019) sp 3 (0.034)

Synedra sp 1 (0.001) Netrium sp 1 (0.004)

Cymbella sp 1 (0.003) Gonatozygon sp 1 (0.012) sp 2 (0.007)

Chlorophyta Mougeotia sp 1 (0.009)

Morpho genera 5 (0.028) and Bulbochaete sp 1 (0.041)

Morpho genera 4 (0.048)

Oil palm with and without buffer strip Bacillariophyta

(5 taxa) Gyrosigma sp 3 (0.002)

Navicula sp 2 (0.006)

Navicula sp 1 (0.004)

Morpho genera 2 (0.005) and

Morpho genera 3 (0.039)

presence in low light conditions (Whitton, 2012;

Komárek & Johansen, 2015). Members of the genus,

Stigonema sp. have been reported in low nutrient

concentration streams (Sagarra, 2017; Schneider et

al., 2013). Additionally, we documented Phormidium

that is a genus that has been widely observed in

periphyton mats, forming dense masses on substrates

such as rocks, plants or in sediments (Azim, 2009;

Komárek & Johansen, 2015). Our results are similar to

those of the species P. autumnale which was reported

in oligotrophic streams with limited light entry (Sagarra,

2017) and low nutrients and temperature (Lindstrøm et

al., 2004).

Our NMDS and subsequent analyses suggested

that communities in pasture streams were affected by

light, NO , and temperature, and were characterized by

16 associated taxa. These streams had the greatest

number of associated taxa, and, in previous work, most

of these taxa have been associated with pollution or

tolerance to high light conditions. For instance, certain

genus of Zygnematophyceae, such as Cosmarium,

Closterium, and Gonatozygon, have been associated

with eutrophic waters with high benthic chlorophyll-a

concentrations (da Silva et al., 2018) as in our study.

Diatoms associated to pasture streams were

Gomphonema sp., Synedra sp., and Cymbella sp.

Many species reported in those genera are associated

in streams with high organic matter concentrations

(Salomoni et al., 2006; Day & Dhlomo, 2007; Daruich et

al., 2013). Some species of Gomphonema have been

associated with pasture streams and coffee plantations

(Vázquez et al., 2011). Synedra species were reported

as primary indicators of anthropogenic eutrophication,

in rivers with organic matter (Maishale & Ulavi, 2015).

Regardless of the genus Cymbella, our results support

those of Tromboni et. al., (2019) who linked the genus

to high light tolerance, and those of Vázquez et al.

(2011) who exclusively found C. tumida in pasture and

coffee plantations streams.

In the streams running through palm oil plantations,

indicator species, such as Navicula sp. and Gyrosigma

sp, are associated with water turbidity. The genus

Navicula includes species adapted to a variety of

habitats (Van Dam et al., 1994), with some known for

their tolerance to turbid conditions (Eloranta &

Soininen, 2002). One species from the Navicula genus

has been reported in urban streams with low oxygen

levels and high biochemical oxygen demand (BOD₅)

(Bere & Tundisi, 2011). Additionally, Navicula have

been identified as pollution-tolerant species (Salomoni

et al., 2006). The genus Gyrosigma also contributed to

the assemblages found in oil palm streams and is

known for its tolerance to disturbed environments. For

example, a Gyrosigma species was reported in

agricultural streams experiencing eutrophic conditions,

with elevated sediment loads and high concentrations

of suspended solids and nutrients (Bona et al., 2007;

Vázquez et al., 2011). Another Gyrosigma species has

Bol. Soc. Zool. Uruguay (2ª época). 2024. ISSN 2393-6940Vol. 33 (2): e33.2.5

VARGAS-LOPEZ et al.

Fig. 4. Nonmetric multidimensional scaling (NMDS) of periphyton density with statistically significant environmental vectors.

Stress value 0.166921. Land cover treatment (forested (FO), oil palm (OP), oil palm with buffer (OPB), and pasture (PA)).

been associated with streams containing elevated

levels of total nitrogen, nitrate, and phosphorus

(Mangadze et al., 2015).

Our work should be considered with the following

limitations in mind. First, we were only able to include a

small number of sites for comparing buffered and

unbuffered oil palm. Additionally, we were limited in our

capacity to collect repeated samples of physico-

chemical data. Our findings may also have been

influenced by the approach we used to identify algal

taxa. In recent years, much of the research on

photosynthetic microorganisms has employed

genomic methods that permit a more robust species

classification compared to traditional morphological

identification (Pawlowski et al., 2022). Here, we used

morphological identification similar to Bere & Tundisi

(2011), Mangadze et al. (2015), Tromboni et al. (2019),

and Vázquez et al. (2011). Errors in identification may

come from the complexities of organism morphologies

and cell structures, which can be challenging to

distinguish without proper microscopes and

specialized expertise in algae taxonomy (Manoylov,

2014). Another important limitation of our study was the

variability in hard substrates in our research sites,

particularly in pasture and oil palm streams. In many of

these streams, stones were absent, requiring us to

collect periphyton from woody substrates. We

acknowledge that this choice could obscure the effects

of land cover, as different algae species exhibit

substrate-specific preferences and introduce bias into

our interpretations (Allan & Castillo, 2021). Future work

in oil palm plantations should employ artificial

substrates, such as unglazed ceramic tiles, to

standardize periphyton collection (Porter-Goff et al.,

2010; Tromboni et al., 2019).

CONCLUSION

This study aimed to elucidate the relationship

between land use, benthic chlorophyll-a concentra-

tions (algae biomass), as well as periphyton richness,

evenness, and community composition. We found that

streams with high canopy cover (forest and oil palm

with buffer strip) had reduced algae biomass compared

to open canopy streams (pasture and unbuffered oil

palm streams). We found no substantial differences in

periphyton taxa richness and diversity between for-

ested areas, oil palm plantations, and oil palm planta-

tions with or without buffer strips. Additionally, we found

that pasture streams changed significantly periphyton

taxa richness and diversity, exhibiting the highest num-

ber of associated taxa known from previous studies to

be linked to pollution or tolerance to high light condi-

tions. While we observed no substantial differences in

taxa richness and diversity between forested streams

and oil palm plantations, the composition of periphyton

communities was notably influenced by land cover.

Specifically, streams affected by oil palm cultivation

hosted more tolerant species, regardless of the pres-

ence of riparian buffers. These results underscore the

complex interactions between agricultural practices

and aquatic ecosystems, challenging our initial expec-

tations regarding the differences between forested and

oil palm-impacted streams. Ultimately, our study con-

tributes to the understanding of how land use alter-

ations affect photosynthetic microorganisms and

emphasizes the need for further research into the eco-

logical implications of oil palm cultivation and agricul-

tural practices on freshwater biodiversity.

Biofilms, which include periphytic algae and

decomposers, contribute to energy flow and

biogeochemical cycling in rivers and often serve as the

foundation of aquatic food webs (Brett et al., 2017; Guo

et al., 2016; Hall & Meyer, 1998; March & Pringle, 2003;

Marks, 2019). Our work documented that one of pri-

mary conservation measures used by plantation man-

agers, the use of riparian buffers (Lucey et al., 2018),

had limited influence on the composition of

photosynthetic microorganisms, despite our small

sample size. Further, research on leaf litter decomposi-

tion within oil palm plantations has yielded mixed

results, with no consistent pattern emerging regarding

the effectiveness of riparian zone conservation to main-

tain ecosystem processes (Chellaiah & Yule, 2018b;

Rojas-Castillo et al., 2024b). This underscores the

need for additional studies focused on both the

autotrophic and decomposer components of biofilms in

oil palm-affected streams. Such research would

deepen our understanding of how palm plantations

impact aquatic ecosystems, and could enhance con-

servation strategies aimed for mitigating the ecological

impacts of continued palm expansion.

ACKNOWLEDGMENTS

We want to thank the personnel of the Lachuá

National Park, and Ricardo Cac for the support and

lessons learned in the field. We appreciate the

collaboration of Hans Graff for allowing us to do

research on his plantation. We are grateful with Centro

de Estudios de Atitlán and Ciencias Biológicas y

Oceanográficas Laboratory for allowing us access to

their facilities for the analysis and identification of

algae. Special thanks to Jose Roberto Ortíz, Estuardo

Bocel, and Jorge García-Polo for their valuable

support. We greatly appreciate the effort of Trine

Warming Perlt from the University of Copenhagen and

Mónica Martínez from the Centro de Estudios de Atitlán

for their help in algae species identification. We want to

acknowledge the feedback provided by Irene Sánchez

on the introduction of the manuscript and express our

deepest appreciation to the Rojas Castillo and Vargas

Bol. Soc. Zool. Uruguay (2ª época). 2024. ISSN 2393-6940Vol. 33 (2): e33.2.5

The influence of land cover on periphyton communities in streams in northern Guatemala

López families for their incredible support and

kindness. This project received funding from the

European Union's Horizon 2020 research and

innovation program under the Marie Skłodowska-Curie

agreement No 801199. We would like to thank

Macrolatinos@ and the reviewers for their important

contributions to this manuscript.

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