Aquatic Toxicology 83 (2007) 223–237
Planktonic microbial community responses to added copper
Anne-H´ el` ene Le Jeune
a,b
, Marie Charpin
a,∗
, Denis Sargos
a
, Jean-Franc ¸ois Lenain
b
,
V´ eronique Deluchat
b
, Nadine Ngayila
b
, Michel Baudu
b
, Christian Amblard
a
a
UMR CNRS 6023, Laboratoire de Biologie des Protistes, Universit´ e Clermont-Ferrand II, 24, avenue des Landais, 63177 Aubi` ere Cedex, France
b
Laboratoire des Sciences de l’Eau et de l’Environnement, Facult´ e des Sciences et Techniques, 123, avenue Albert-Thomas, 87060 Limoges Cedex, France
Received 24 January 2007; received in revised form 11 April 2007; accepted 27 April 2007
Abstract
It is generally agreed that autotrophic organisms and especially phytoplanktonic species can be harmed by copper through its effect on photo-
system. However, the impact of copper on other components of the pelagic food web, such as the microbial loop (autotrophic and heterotrophic
picoplankton, pigmented and non-pigmented flagellates and ciliates) has received little attention. Indoor experiments were conducted to evaluate
the direct and indirect effects of copper, supplied in the range of concentrations used to control cyanobacteria growth in ponds, on non-targeted
organisms of natural microbial loop communities sampled in spring and summer. Two copper concentrations were tested (80 gL
-1
and 160 gL
-1
final concentrations), set, respectively, below and above the ligand binding capacity of the water samples. Both caused a significant decrease in the
biomass and diversity of pigmented organisms (picophytoplankton and pigmented flagellates). Conversely, the heterotrophic bacterioplankton and
the heterotrophic flagellates did not seem to be directly affected by either copper treatment in terms of biomass or diversity, according to the descrip-
tor chosen. The ciliate biomass was significantly reduced with increasing copper concentrations, but differences in sensitivity appeared between
spring and summer communities. Potential mixotrophic and nanoplanktorivorous ciliates appeared to be more sensitive to copper treatments than
bacterivorous ciliates, suggesting a stronger direct and (or) indirect effect of copper on the former.
Copper sulphate treatments had a significant restructuring effect on the microbial loop communities, resulting in a dominance of heterotrophic
bacterioplankton among microbial microorganisms 27 days after the beginning of the treatment. The spring microbial communities exhibited a
greater sensitivity than the summer communities with respect to their initial compositions.
© 2007 Elsevier B.V. All rights reserved.
Keywords: Microbial loop; Copper; Pigmented organisms; Non-pigmented organisms
1. Introduction
Copper sulphate treatments have long been used to control
phytoplanktonic biomass (Haughey et al., 2000), by virtue of the
high sensitivity of autotrophic organisms to cupric ions (Sunda
and Lewis, 1978). With the rising frequency of Cyanobacteria
blooms, this type of treatment is still largely employed at the
early stage of bloom formation in ponds used for recreational
activities to avert potential human exposure to cyanotoxins.
The effects of copper sulphate on single autotrophic species
(toxicity tests) and phytoplanktonic communities (field stud-
ies) have been well researched (McKnight, 1981; Winner and
Owen, 1991; Gustavson and W¨ angberg, 1995; Franklin et al.,
2002; Peˇ na-Castro et al., 2004; Soldo et al., 2005; Le Jeune et
∗
Corresponding author. Tel.: +33 4 73 40 77 12; fax: +33 4 73 40 76 70.
E-mail address: Marie.CHARPIN@univ-bpclermont.fr (M. Charpin).
al., 2006). In contrast, little work has been reported on its effects
on non-targeted organisms. In freshwater media, the food web
interactions among autotrophic and heterotrophic bacteria and
their protozoan grazers (flagellates and ciliates) recycle particu-
late and soluble nutrients released by the classical pelagic food
chain (phytoplankton, zooplankton, fish) (Azam et al., 1983).
This complementary trophic food chain, called the microbial
loop, can act as a significant mediator of energy transfer to
upper trophic levels by recovering part of the pelagic produc-
tion that would otherwise be lost from the systems (Amblard et
al., 1998). Trace elements such as copper sustain essential key
metabolic functions in a wide range of organisms, but exces-
sive concentrations can cause adverse toxic effects (Bar´ on et al.,
1995). The picoplankton (auto- and heterotrophic bacteria) have
been thought to play an important role in the trophic transfer of
trace elements by scavenging dissolved trace metals through
their high surface-area-to-volume ratios (Twiss and Campbell,
1995; Twiss et al., 1996). In the case of rising concentrations of
0166-445X/$ – see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquatox.2007.04.007