Periphyton and phytoplankton associated with the tropical carnivorous

plant Utricularia foliosa

Jhon Dıaz-Olarte a, Vanessa Valoyes-Valois b, Castor Guisande c,*, Nestor Ned Torres d,Adriana Gonzalez-Bermudez e, Lizandro Sanabria-Aranda a, Ana M. Manjarres Hernandez f,

Santiago R. Duque d, Lili J. Marciales d, Marcela Nunez-Avellaneda g

a Facultad de Ciencias, Escuela de Biologıa, Universidad Industrial de Santander, 678 Bucaramanga, Colombiab Facultad de Ciencias Basicas, Universidad Tecnologica del Choco Diego Luis Cordoba, Quibdo, Colombia

c Facultad de Ciencias, Universidad de Vigo, Campus Lagoas-Marcosende, 36200 Vigo, Spaind Instituto Amazonico de Investigaciones-IMANI, Universidad Nacional de Colombia, km 2 vıa Tarapaca, Leticia, Colombia

e Facultad de Ciencias y Educacion, Universidad Distrital Francisco Jose de Caldas, 8668 Bogota, Colombiaf Grupo de Investigaciones en Cuencas y Humedales Tropicales, Universidad del Magdalena, 10004 Santa Marta, Colombia

g Instituto Amazonico de Investigaciones Cientıficas Sinchi, Leticia, Colombia

Received 20 February 2007; received in revised form 27 June 2007; accepted 29 June 2007

Available online 4 July 2007

Abstract

The abundance and taxonomic composition of periphyton attached to the bladders and phytoplankton associated with the aquatic carnivorous

plant Utricularia foliosa were quantified, to determine whether periphyton associated with U. foliosa would enhances predation success. Bladder

size, periphyton abundance and periphyton richness together explained 76% of the variation observed in the number of prey captured by the

bladders. The abundance and richness of periphyton followed the same pattern as phytoplankton, i.e., both increased as dissolved inorganic

phosphate concentration rose. This nutrient concentration explained 84 and 74% of the variation observed in richness and abundance of periphyton,

respectively. This suggests that abundance and richness of the periphyton associated with U. foliosa depend mostly on environmental conditions rather

than on facilitation mechanisms displayed by the plant. In conclusion, if periphyton affects U. folisosa negatively due to the competition for light or

nutrients, the plant is ‘‘fated to get along with the enemy’’ but apparently without the capacity to manipulate this ‘‘enemy’’ to its own advantage.

# 2007 Elsevier B.V. All rights reserved.

Keywords: Phytoplankton; Periphyton; Bladderwort; Aquatic carnivorous plant; Zooplankton; Nutrient

1. Introduction

The selective capture by Utricularia of prey from a wide

array of aquatic invertebrates is selective, since the percentage

of species captured by bladders is different from that in the

habitat (Harms, 1999; Jobson and Morris, 2001; Guisande et al.,

2000, 2004). Although this may be due to either the behavior of

some prey that swim close to the bladders looking for the food

attached to them or to the plant’s prey-attracting mechanisms,

the evolution of the latter is implied by the relative contribution

of prey nitrogen to total nitrogen content estimated at 51.8% in

Utricularia vulgaris (Friday and Quarmby, 1994).

* Corresponding author. Tel.: +34 986 812586; fax: +34 986 812556.

E-mail address: castor@uvigo.es (C. Guisande).

0304-3770/$ – see front matter # 2007 Elsevier B.V. All rights reserved.

doi:10.1016/j.aquabot.2007.06.010

However, the only strategy observed so far for luring prey is

the presence of antennae and bristles that probably lead

potential substratum-dwelling prey towards the valve used by

Utricularia spp. for trapping prey (Meyers and Strickler, 1979;

Sanabria-Aranda et al., 2006). Although it is suspected that

Utricularia spp. additionally employ one or more chemo-

attraction strategies to lure prey, so far none have been

satisfactorily demonstrated (Guisande et al., 2000, 2004;

Manjarres-Hernandez et al., 2006). Early hypotheses postulat-

ing the attraction of prey via the production of carbohydrates on

the valve (Cohn, 1875; Meyers, 1982; Luetzelburg, 1910) have

been rebutted by later studies (Meyers and Strickler, 1979;

Sanabria-Aranda et al., 2006).

An alternative chemical mechanism evolved to lure prey

may be to enhance periphyton quality or quantity, which might

attract grazing zooplankton and macroinvertebrates close to the

trap door. Since the composition of algal periphyton can vary

among different aquatic plant hosts (Blindow, 1987), the host

might manipulate the periphyton community to its own

advantage (Jones et al., 1999). Using surface texture or

chemical control, such as allelopathic substances influencing

algal growth (Gross et al., 2007), the host might enhance

periphyton abundance or favor highly edible and nutritious

periphyton species. Evidence that these periphyton biomass

enhancing mechanisms might be operative in Utricularia

include a model showing that the plant harnesses the production

of its own periphyton via intermediary grazers (Ulanowicz,

1995) and the greater abundance and diversity of periphyton

found on Utricularia relative to sympatric macrophytes

(Bosserman, 1983).

Information about the periphyton and phytoplankton

associated with aquatic carnivorous plants is scarce, although

in Utricularia foliosa desmids have been described as the most

abundant group, followed by Chlorococcales and Cyanophyta

(Lacoste de Diaz, 1981; Wagner and Mshigeni, 1986).

However, there are no studies on spatial or temporal changes

in abundance or composition of the periphyton associated with

bladders according to changes in the water quality, nor are there

studies to determine whether prey captured or prey abundance

around the plant is related to periphyton abundance and

composition associated with the bladders. In this study, we

examined these aspects with respect to U. foliosa located in

Yahuarcaca creek and lake (Colombian Amazon), with the aim

of determining whether the plants manipulate periphyton

community abundance or composition to their own advantage.

2. Materials and methods

Sampling was carried out five times from March 21 to

May 30 2005 from seven plants of U. foliosa growing in

seven different places along the Yahuarcaca creek and lake

in the Colombian Amazon, from closest to furthest from the

river: site 1 (4810012.200S, 69857038.200W), site 2 (489058.700S,

69857048.300W), site 3 (489036.800S, 6985800.0500W), site 4

(489029.100S, 6985800.0500W), site 5 (489016.200S, 69858010.700W),

site 6 (489018.900S, 6985800.0900W) and site 7 (48904.1.00S,

6985703800W). The sampling was carried out during the growing

season of the plant. This species occurs in the field (mainly from

March to May), just when the wet season begins and water from

the Amazon starts to enter the lakes and creeks.

Each sampling day we randomly collected three leaves of

each plant. Because each plant covers between 4 and 18 m2 in

surface and grows 1–4 m deep, the sampling was not detrimental

to the plant. The age of the leaf was not taken into account when

collecting the bladders. From each leaf, 50 bladders were also

randomly collected to determine the size distribution of bladders

with and without prey and the kind and number of prey captured

by the plant. Bladder size was quantified as the greatest length

from stalk end to the trap-door end.

Each sampling day, two quantitative samples of phyto-

plankton were taken, one at 0.5 m inside and the other 0.5 m

outside of each plant with a 2.5 L Van Dorn bottle. The samples

were preserved with Lugol’s solution. The abundance of each

species was determined by Utermohl’s method using 50 or

100 mL depending on the plankton abundance. Census was

halted when 100 units (cells, colonies or filaments) of the most

abundant species had been counted.

Periphyton associated with the bladders of each leaf was

analysed by five randomly collected bladders from different

size ranges: 800–1000, 1000–1200, 1200–1400, 1400–1600,

1600–1800 and 1800–2000 mm. The periphyton associated

with each set of five bladders were removed by scraping, and

later the bladders were gently broken using two needles and

preserved in an eppendorf vial with 1.5 mL of Lugol solution.

The periphyton was removed from surfaces of the bladders by

vigorous manual shaking in 1.5 mL Lugol solution during

3 min, which was confirmed by visual inspection of the

bladders. The abundance of each species was determined by

counting the entire 1.5 mL volume of Lugol under direct

microscope. In order to identify diatom species, samples were

treated to eliminate organic matter following the method

described by Hasle and Frixell (1970), using hot H2O2 before

mounting for observation. Observations were carried out with

an Olympus CH-2 microscope (400�).

Quantitative zooplankton samples were collected inside the

plant stand at the same places after collecting the phytoplankton

and periphyton samples. Samples were taken from 0.5 m depth

with a 20 L Schindler–Patalas plankton trap. The plant was

shaken strongly in the water before taking the zooplankton

sample inside the plant to collect both free-swimming and epi-

phytic zooplankton. The 20 L sample was concentrated through a

20 mm mesh net and preserved in 100 mL 4% formaldehyde

solution. Estimates of the abundance of zooplankton were made

by counting the quantitative samples using an inverted

microscope at 100� magnification. For each sample, at least

25% of the volume of the quantitative sample was examined.

At a depth of 0.5 m the oxygen concentration, pH,

conductivity, temperature, ammonia (NH4+), nitrate (NO3

�),

nitrite (NO2�), silicate (SiO4

�) and phosphate (PO43�) were

measured inside the plant and outside the plant for the seven

plants. Filtered water (0.45 mm) was used for measuring

nutrients with BRAN + LUEBBE AAIII autoanalyser.

The software used for the statistical analyses was SPSS (SPSS

Inc. 2003) and STATISTICA (Statsoft, 2004). Autocorrelation

among residuals and co-linearity among independent variables

was tested in the regression analyses (Guisande et al., 2006).

3. Results

3.1. Concentration of nutrients

The concentrations of both NO3� and PO4

3� were low in all

locations (Manjarres-Hernandez et al., 2006). The concentra-

tion of NO3�was lower in areas closer to the Amazon River and

higher in the areas more influenced by the creek, whereas the

concentration of PO43� showed an opposite pattern, being

higher in the areas closer to the Amazon River. The

concentration of SiO4� was high in all locations and hence,

diatoms were probably not limited by inorganic silicium

(Manjarres-Hernandez et al., 2006).

Fig. 1. Mean percentage abundance � S.D. over sampling period and the sites

of the different phytoplankton orders inside and outside the plant.

Fig. 2. Comparison inside and outside the plant for (a) phytoplankton abun-

dance and (b) phytoplankton richness. The line represents the situation with the

same abundance or richness inside and outside the plant.

Fig. 3. Relationship between PO43� concentration and the means � S.D. of

phytoplankton abundance (open symbols) and phytoplankton richness (filled

symbols) inside (circles) and outside (triangles) the plant, in the sites where the

plants where collected.

3.2. Phytoplankton

The phytoplankton community, both inside and outside the

plant, consisted of Oscillatoriales (Cyanophyta), Desmidiales

(Zygophyta), Euglenales (Euglenophyta), Chlorococcales

(Chlorophyta), Pennales and Centrales (Bacillariophyta)

(Fig. 1). Phytoplankton richness and abundance was higher

inside the plant than outside (Fig. 2). Phytoplankton richness and

abundance increased with PO43� concentration both inside and

outside the plant (Fig. 3). PO43� concentration explained 83%

(slope different from zero, F1,5 = 23.6, r2 = 0.83, P = 0.005) and

82% (slope different from zero, F1,5 = 22.3, r2 = 0.82,

P = 0.005) of the variation observed in the richness of

phytoplankton inside and outside the plant, respectively, and

95% (slope different from zero, F1,5 = 98, r2 = 0.95, P < 0.001)

and 73% (slope different from zero, F1,5 = 13.7, r2 = 0.73,

P = 0.014) of the variation observed in the abundance of

phytoplankton inside and outside the plant, respectively. An

analysis of covariance, taking PO43� concentration as covari-

able, showed significant differences in phytoplankton abundance

(F1,67 = 13.1, P < 0.001) and phytoplankton richness (F1,67 =

13.1, P = 0.004) between inside and outside the plant. Diversity

increased mainly in Desmidiales and Chlorococcales with PO43�

concentration, both inside and outside the plant (Fig. 4).

3.3. Periphyton

The most abundant algae taxa in the periphyton community

attached to the bladders were similar to those that dominated in

Fig. 4. Relationship between PO43� concentration and the mean � S.D. rich-

ness of Desmidiales and Chlorococcales in the phytoplankton inside (circles)

and outside (triangles) the plant, in the sites where the plants were collected.

Fig. 5. Mean � S.D. percentage abundance over the sampling period and in the

different sites of the different periphyton order attached to the bladders of the

plants.

Fig. 6. Relationship between PO43� concentration and the means � S.D. over

the sampling period of the periphyton abundance (open symbols) and richness

(filled symbols) of periphyton attached to the different plants. The solid line

shows the regression between PO43� concentration and periphyton richness.

the phytoplankton community: Oscillatoriales, Desmidiales,

Chlorococcales, Pennales and Centrales (Fig. 5). A discriminant

analysis performed on the data of periphyton richness showed

that it was possible to discriminate among plants, because 100%

of the cases were correctly classified. Only the discriminant

function I was statistically significant (Lambda of Wilks = 0.003,

P = 0.013), and discriminates mainly among those plants located

in sites with low PO43� (sites 6 and 7) and high PO4

3� (site 2).

Therefore, similar to the pattern observed with phytoplankton,

periphyton richness and abundance increased with PO43�

concentration (Fig. 6). Pennales, Euglenales and Oscillatoriales

were the periphyton taxa that mainly increased their richness

with PO43� concentration (Fig. 7). PO4

3� concentration

explained 84% (slope different from zero, F1,5 = 26.6,

r2 = 0.84, P = 0.004) and 74% (slope different from zero,

F1,5 = 14.1, r2 = 0.74, P = 0.013) of the variation observed in the

richness and abundance of periphyton, respectively.

In addition to the covariance with PO43� concentration, the

abundance (Fig. 8) and richness (Fig. 9) of the periphyton

increased with bladder length. A stepwise regression showed

that bladder length (in mm, log transformed) and PO43�

concentration (in mM) explained 51% of the variation observed

in the abundance (Table 1 F1,40 = 22.6, r2 = 0.51, P < 0.001)

and 61% of the variation observed in the richness (Table 2)

F1,40 = 33.7, r2 = 0.61, P < 0.001) of the periphyton.

3.4. Zooplankton

The zooplankton community associated to the plants was

described in Sanabria-Aranda et al. (2006). A discriminant

analysis performed on the data of zooplankton richness inside

the plant showed that it was not possible to discriminate among

plants, because all discriminant functions were statistically not

significant (Lambda of Wilks >0.4, P > 0.56). Moreover, no

significant relationship was found between periphyton abun-

dance per bladder and zooplankton abundance inside the plant

(F1,33 = 2.7, r2 = 0.08, P = 0.109), or between periphyton

richness per bladder and zooplankton richness inside the plant

(F1,33 = 0.8, r2 = 0.02, P = 0.376).

Fig. 7. Relationship between PO43� concentration and the mean � S.D. rich-

ness over the sampling period of Euglenales, Pennales and Oscillatoriales in the

periphyton attached to the bladders of the different plants.

Fig. 8. Relationship between mean bladder length and the mean abundance of

periphyton over the sampling period attached to the bladders of the different

plants. Symbols as mentioned in Fig. 2.

Fig. 9. Relationship between mean bladder length and the mean richness of

periphyton over the sampling period attached to the bladders of the different

plants. Symbols as mentioned in Fig. 2.

3.5. Relationship between the composition and abundance

of periphyton and predation success

The number of prey captured by bladders rose as bladder

length increased (Fig. 10), which covariates with periphyton

abundance and richness associated with bladders, hence

possibly enhancing the capacity of bladders to lure prey,

because predation efficiency, i.e., prey captured for a given

bladder size, assuming that ‘‘efficiency’’ means more prey

captured for a given bladder size, increased with periphyton

abundance and richness (Fig. 10). A stepwise regression

showed that bladder length (in mm, log transformed),

periphyton abundance per bladder and periphyton richness

per bladder together explained 76% of the variation observed in

the mean number of prey captured per bladder by each plant

over the sampling period (Table 3). Bladder length explained

most of the variance, but periphyton added a significant

proportion (Table 3). Neither autocorrelation among residuals

(Durbin–Watson = 1.7) nor colinearity among independent

variables (variance inflation factors for all independent

variables were lower than 2.4) were observed.

We found no apparent relationship between periphyton

richness and abundance with zooplankton richness and

Table 1

Results of the stepwise regression taking abundance of periphyton as the

dependent variable, and bladder length (ln transformed) and PO43� concentra-

tion as independent variables

Variable Cumulative

explained variance

Coefficient � S.E. P

Constant �236.4 � 41.5 0.001

Ln (bladder length) 0.42 34.2 � 5.6 0.001

PO43� concentration 0.51 108.4 � 36.9 0.006

Fig. 10. Relationship between the mean number of prey captured by bladders

and the mean bladder length, with indication of the mean periphyton abundance

and richness for each plant. Symbols as mentioned in Fig. 2.

Table 3

abundance (see above). Therefore, an increased capture of

preys by bladders as periphyton abundance and richness cannot

be explained by a higher abundance of prey available.

4. Discussion

The presence of a layer of periphyton on the submerged parts

of aquatic plants reduces light and carbon availability and may

enhance competition for nutrients (Jones et al., 1999).

Therefore, this periphyton appears detrimental to its host

plant. It has been suggested that submerged aquatic plants can

influence the nutritional quality of attached periphyton, making

it more nutritious for grazing invertebrates (Thomas, 1990). In

return, the grazers might preferentially feed on the periphyton

and clear the plants of a potential competitor, with the plants

and grazers both gaining from this mutualistic relationship. The

potential influence of the plant on periphyton quality and

quantity might be a mechanism evolved to lure prey.

The result of the interaction with the animals seems only

positive for the plant. Zooplankton and macroinvertebrates

favor carnivorous plants by grazing on periphyton and also

because the animals are the plant’s food. However, despite our

observation that periphyton abundance and richness enhance

predation success, the results of this study show that spatial

changes in the abundance of the periphyton associated with U.

foliosa depend mostly on environmental conditions (such as

PO43� concentration), which has been observed in Utricularia

and other submerged aquatic plants (Jones et al., 1999; Havens

et al., 1999; Hillebrand and Kahlert, 2001; Englund and Harms,

2003; Hillebrand, 2003), rather than on a facilitation

mechanism displayed by the plant. Although Jones et al.

(1999) showed that submerged aquatic plants exert a

considerable influence over their periphyton, either actively

or passively, they found no evidence that plants manipulate the

periphyton to encourage periphyton grazers, concluding that

there was no co-evolved mutualism. The fact that the

abundance of the periphyton associated with U. foliosa depend

Table 2

Results of the stepwise regression taking richness of periphyton as the depen-

dent variable, and bladder length (ln transformed) and PO43� concentration as

independent variables

Variable Cumulative

explained variance

Coefficient � S.E. P

Constant �30.2 � 12.9 0.024

Ln (bladder length) 0.58 90.9 � 11.5 0.001

PO43� concentration 0.61 3.8 � 1.7 0.034

mostly on changes in PO43� concentration seems to confirm

this: also U. foliosa does not exert an active influence to

enhance periphyton quality and quantity as a mechanism

evolved to lure prey.

Suppression of plant growth by periphyton has been

demonstrated in many studies (Sand-Jensen, 1977; Sand-

Jensen and Søndergaard, 1981; Jones and Sayer, 2003),

demonstrating the negative effect of periphyton on aquatic

plants. It has been shown that there is competition between

macrophytes and periphyton for nutrients and light (Carpenter

and Lodge, 1986; Sand-Jensen and Borum, 1991; Jobson et al.,

2000), indicating a negative effect of the periphyton on

Utricularia. Therefore, our findings suggest that the interaction

between U. foliosa and periphyton is also positive for the

carnivorous plant, particularly under nutrient limitation. With

little or no periphyton, the traps lure less prey (Fig. 10). These

results agree with the study of Ulanowicz (1995), who showed

with a model that Utricularia harnesses the production of its

own periphyton via intermediary grazers. Therefore, if we

assume, based on previous studies (Carpenter and Lodge, 1986;

Sand-Jensen and Borum, 1991), that periphyton affects U.

folisosa negatively due to the competition for light or nutrients,

U. foliosa is ‘‘fated to get along with the enemy’’ but apparently

without the capacity to manipulate the ‘‘enemy’’ to its own

advantage. However, it is necessary to point out that our field

studies are based on correlations, not on experimental

manipulation. Therefore, it is not possible reject the hypothesis

Results of the stepwise regression taking number of preys captured per bladder

as the dependent variable, and bladder length (ln transformed), periphyton

abundance per bladder and periphyton richness per bladder as independent

variables

Variable Cumulative

explained variance

Coefficient � S.E. P

Constant �11.1 � 1.7 0.001

Ln (bladder length) 0.52 1.53 � 0.25 0.001

Periphyton richness 0.73 0.13 � 0.02 0.001

Periphyton abundance 0.76 0.01 � 0.005 0.05

that the bladders with more periphyton have more prey, not

because of the periphyton, but because of something associated

with more periphyton. Experimental manipulation would be

necessary to corroborate these correlations observed in the

field.

This study supports the need of a tri-trophic perspective,

rather than bi-trophic perspective based on either plant–

herbivore or herbivore–carnivore interactions alone (Singer and

Stireman, 2005).

Acknowledgements

We thank the Universidad Nacional de Colombia Sede

Amazonia, XUNTA de GALICIA and the University of Vigo

for financial support, and to Allan Wood for useful comments

on the manuscript.

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