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LIMNETIC ZOOPLANKTON OF CHILEAN LAKES AND RESERVOIRS:
A TRIBUTE TO BERNARD DUSSART
VIVIAN MONTECINO1,3 ), JUAN PABLO OYANEDEL1 ), IRMA VILA1 )
and LUIS ZÚÑIGA2 )
1 ) Departamento de Ciencias Ecológicas, Facultad de Ciencias Universidad de Chile,
Santiago, Chile
2 ) Instituto de Biología, Facultad de Ciencias Básicas y Matemáticas, Pontificia Universidad
Católica de Valparaíso, Chile
ABSTRACT
Knowledge of Chilean freshwater zooplankton has substantially accelerated since the
development of the Man and Biosphere (MAB) — UNESCO Program, from 1975 onwards.
One of the specialists who took part in this program was Bernard Dussart. We present
a synthetic picture of Dussart’s contribution to these local studies, and the more recent regional
understanding of zooplankton components in natural and man-made lakes. Information on
zooplankton taxonomy and ecology has increased noticeably during the last three decades, from
two or three publications per decade, to one per year. This has permitted a more thorough
insight into latitudinal trends in the distribution of copepods and branchiopods, the latter
having an overall higher species richness and with a greater presence in reservoirs or more
temperate and eutrophic systems. Maximum zooplankton species richness at approximately
40◦ S also encompasses a higher percentage of copepods, as latitude and the proportion
of oligotrophic water bodies increase. This latitudinal distribution and the species richness
pattern are unaffected by the more recent surveys of the planktonic crustacean communities.
These surveys and other ecological studies have provided a further and thorough insight into
freshwater system components and the environmental relationships of the limnetic biota.
RÉSUMÉ
La connaissance sur le zooplancton des eaux douces chiliennes s’est considérablement
accélérée depuis le développement du programme Man and Biosphere (MAB) — UNESCO,
à partir de 1975. L’un des spécialistes qui prirent part à ce programme était Bernard Dussart.
Nous présentons ici une vue synthétique de la contribution de B. Dussart à ces études locales,
et l’état le plus récent de nos connaissances concernant les composants du zooplancton dans
les lacs naturels et artificiels de la région. L’information sur la taxonomie et l’écologie du
zooplancton s’est accrue sensiblement au cours des trois dernières décennies, de deux à trois
publications par décennie à une par an. Ceci a permis une perception plus approfondie des
3 ) Corresponding author; e-mail: [email protected]
© Koninklijke Brill NV, Leiden, 2011
Studies on Freshwater Copepoda: 355-369
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influences latitudinales sur la répartition des copépodes et des branchiopodes, ces derniers
montrant la plus grande richesse globale en espèces et une présence plus importante dans
les réservoirs ou les systèmes plus tempérés et eutrophes. La richesse spécifique maximale
du zooplancton aux environs de 40◦ S comprend un pourcentage plus élevé de copépodes,
quand la latitude et la proportion des collections d’eaux oligotrophes augmentent. Cette
répartition latitudinale et le patron de richesse spécifique n’ont pas été modifiés après les
études les plus récentes sur les communautés de crustacés planctoniques. Ces travaux ainsi
que d’autres études écologiques ont fourni une perception plus approfondie et complémentaire
des composants des écosystèmes aquatiques et des relations de la biodiversité des eaux douces
avec l’environnement.
INTRODUCTION
Bernard Dussart’s academic exchanges with South American and Chilean
colleagues were seminal contributions to the development of Chilean limnology. Dussart’s first visit to Chile was on the occasion of the “International
Workshop in Limnology and Integrated Management of Reservoirs” held in
Santiago in 1979, organized by the Universidad de Chile and the UNESCO
Man and Biosphere (MAB) Program. Bernard Dussart was invited as an expert
to lead a conference on the effects of impoundments, for an emerging group of
specialists and young students (fig. 1). As a result of this workshop, the book
“Embalses, Fotosíntesis y Productividad Primaria” was published (edited by
Bahamonde & Cabrera, 1984) and freely distributed in Chile and South America, also financed by the UNESCO-MAB Program. This book has served many
generations of students in Limnology and Marine Sciences in the region.
Further, and as a consequence of his contact with colleagues, lecturers,
and the student participants in this workshop, Dussart worked on material
that he collected during his stay in Chile (Dussart, 1979). Dussart also
developed research links with the Chilean carcinologists Nibaldo Bahamonde
and Rosario Ruíz in Santiago, and the Argentinian Silvina Menu-Marque,
reinforcing the work of other scientists, mostly Prof. Luis Zúñiga in Valparaíso
and all the contemporaneous and later students: Doris Soto, Boris Villalobos,
and Lorena Villalobos among others (see References).
Bernard Dussart’s taxonomic work on freshwater copepods is recognized
worldwide, and South America, particularly Chile, is no exception. He described the diaptomid Tumeodiaptomus vivianae Dussart, 1979 (Dussart,
1979) from Rapel Reservoir (34◦ 02 S 71◦ 35 W), and later transferred to this
genus Diaptomus diabolicus Brehm, 1935 (cf. Dussart & Defaye, 2002).
Concurrently, the geographic distribution of Branchiopoda and Copepoda of
Chilean freshwaters was updated by Ruiz & Bahamonde and published in
1989.
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Fig. 1. Photograph of lecturers and students of the International Workshop in Limnology and
Integrated Management of Reservoirs, Santiago, Chile, October 1979. Among participants are,
as indicated: 1, Morris Assael; 2, Sergio Cabrera; 3, Jorge Cabrera; 4, Rosario Ruiz; 5, Gonzalo
Gajardo; 6, Irma Vila; 7, Bernard Dussart; 8, Manuela Pinto; 9, Laura Huaquin; 10, Silvina
Menu-Marque; 11, Luis Zuñiga; 12, Teresa Donoso; 13, Vivian Montecino; 14, Pedro Valdivia;
15, Matilde Lopez; 16, Raul Ringuelet; 17, Everett Fee; 18, Nibaldo Bahamonde; 19, Heinz
Löffler; 20, Richard Tubb; 21, Victor Dellarossa; 22, Patricio Dominguez; 23, Jairo Valderrama.
Although Dussart’s international importance will be thoroughly reviewed
in this volume, Luis Zúñiga and his former students want to recognize the
fact that for young scientists, his monographs on the Copepoda played a key
role in their orientation. After the 1979 international workshop, academics and
students at the Biological Institute of the Pontificia Universidad Católica de
Valparaíso increased their interest and studies on the structure and distribution
of zooplankton in lakes and reservoirs, and this is reflected in the works by
Zúñiga & Araya (1982), Araya & Zúñiga (1985), Zúñiga (1988), SchmidAraya (1991), Soto & Zúñiga (1991), and Schmid-Araya & Zúñiga (1992).
Although by 1990, limnological studies began to be more experimental,
young scientists did not abandon their interest in zooplankton community
structure, and continued to produce descriptive studies, as shown in the
publications by Villalobos (2006), De los Ríos & Soto (2006, 2007), CarvajalSalamanca et al. (2008), Oyanedel et al. (2008), and De los Ríos & RomeroMieres (2009).
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Since 1980, limnological research at various national centres developed and
contributed to the local or regional understanding of limnetic zooplankton
structure and abundance (Campos, 1984; Soto et al., 1984; Vila et al., 1986;
Andrew et al., 1989; Montecino et al., 1991; Parra et al., 2003). These natural
and man-made lakes in the Chilean territory, including Antarctica, are distributed from approximately 17◦ S to 63◦ S and from sea level to >4000 m asl.
The country being a very narrow territory of western South America, the valleys and coastal lakes are influenced by a common forcing variable, the maritime climate, together with very different north-south precipitation patterns
(fig. 2). This directly influences their seasonal temperature dynamics compared
to systems of similar latitudes in the northern hemisphere; most of these lakes
are temperate monomictic. Their altitudinal gradients in central Chile motivated and enhanced the development of a multidisciplinary limnological pilot
project for the characterization of temperate lakes within the framework of the
UNESCO MAB Program (Vila, 1980; Montecino & Cabrera, 1984; Vila et
al., 1986). During the same period, Campos (1984) characterized the south-
Fig. 2. The six hydrological-climatic zones (arrows) in Chile (top) correspond from north to
south to: HP = High Plateau; WT1 = Warm-temperate with winter rains; WT2 = Warmtemperate with Mediterranean influence; WT3 = Warm-temperate and rainy without dry
season; CS = Cold semi-arid with winter rains; CT = Cold-temperate and rainy without
dry season. These zones are based on Niemeyer & Cereceda (1984) and on the precipitation
averages up to >5000 mm from 1950-2000 (http://www.worldclim.org/), which are coded
according to the insert black–grey scale (bottom left). Chile’s south-west location along N–S
South America is also highlighted and shown in darker grey (bottom right).
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Montecino et al., ZOOPLANKTON OF CHILEAN LAKES AND RESERVOIRS
359
ern oligotrophic piedmont lakes. The latitudinally related factors that regulate
freshwater primary productivity (Montecino, 1991) may be related to trophic
patterns, zooplanktonic species richness, and also their annual variations and
the increasing maritime influence at the more southern latitudes (Soto, 2002).
The goal of this manuscript is to present a general analysis of Chilean
limnology, using data and information on crustacean zooplankton (Copepoda
and Branchiopoda) promoted by the early influence of Bernard Dussart. Whilst
novel ideas are discussed, the zooplankton information collected since then
(the late 1970s) is here described and synthesized for the range of hydrological
and climatic zones in Chile.
METHODS
Crustacean zooplankton information for the present work was analysed
from a matrix constructed from the presence/absence data of the taxa, with
species as columns and sites as rows, to obtain species richness for each site.
These data were taken from Oyanedel et al. (2008) complemented by data
given by De los Ríos (2008) and based on a total of 28 publications (fig. 3).
Consequently, the expansion of limnological research in Chilean fresh waters
can be seen past 1960-1970s, with foreign expeditions and the pioneering
publications of Löffler (1961, 1962, 1966), Thomasson (1963), and Pezzani
(1977).
The origin of these data is a compilation for a range of climatic regions
described for the country by Niemeyer & Cereceda (1984), and a range of
sampling sites, covering the northern high mountain arid region to the southern
humid lake zone, excluding saline lakes. From this matrix, the zooplankton
distribution, starting at the high plateau (HP) northern zone and extending to
the cold semiarid (CS) and cold temperate (CT) Patagonian zones (fig. 2), is
evaluated.
Assessment of total species richness of Copepoda and Branchiopoda among
lakes and reservoirs is carried out with an analysis of covariance (ANCOVA),
in order to minimize the effect of the area of each water-body on species richness. Non-homogenized variances were transformed by square root, according
to Statistical 6.0, StatSoft, Tulsa, Oklahoma.
RESULTS
Based on the number of publications before and after 1980, by 10-year
periods, we found that studies on zooplankton taxonomy increased during the
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Fig. 3. Cumulative number of publications on zooplankton in ten-year periods from 1960
to 2009.
TABLE I
Taxonomic classification, family names, and species numbers of planktonic crustacean zooplankton in Chilean lakes and reservoirs between 18◦ S and 54◦ S
Major group
Class
Order
Family
Crustacea
Copepoda
Calanoida
Branchiopoda
Cyclopoida
Ctenopoda
Anomopoda
Centropagidae
Diaptomidae
Cyclopidae
Sididae
Bosminidae
Chydoridae
Daphniidae
Macrothricidae
Species
15
2
16
2
3
15
15
6
last three decades, from two or three publications in the first two periods to
approximately one per year (fig. 3).
The taxonomic composition of the limnetic crustacean zooplankton of
Chilean fresh waters (table I) recently studied by Villalobos (2006) and Oyanedel et al. (2008) indicates that species richness for the class Branchiopoda
is 41 species in two orders, Ctenopoda (one family) and Anomopoda (four
families). For the class Copepoda there are a total of 33 species in two orders, Calanoida (two families) and Cyclopoida (one family). Taxa of the class
Harpacticoida have been excluded for being benthic and because of lack of information, although Löffler (1961, 1962, 1966) and next Ebert & Noodt (1975)
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Fig. 4. Copepoda and Branchiopoda species richness (%) in the six hydrological-climatic
zones in Chile. The numbers inserted in each column show the total amount of species per
hydrological zone.
found and described a large number of species of zooplankton of Chilean lakes
and reservoirs within the copepod genus Attheyella. Species richness in the six
different hydrological-climatic zones (fig. 2) clearly shows a higher presence
of Branchiopoda in the first two northern zones, whereas in the others there is
a higher presence of Copepoda (fig. 4).
Comparing the overall abundance of total crustacean zooplankton from
lakes and reservoirs (fig. 5), there are no differences between them (ANCOVA
F = 1.518; p = 0.23). When Branchiopoda and Copepoda are treated
separately, there is a higher presence of Branchiopoda in man-made lakes
(ANCOVA F = 4.568; p = 0.046), whereas in the Copepoda no differences
are found (ANCOVA F = 2.795; p = 0.111).
The latitudinal distribution of limnetic zooplankton species richness reported by Soto & Zúñiga (1991) is herein complemented with the current data
(fig. 6). Although an increase in maximum species richness can be detected
around 40◦ S, this comparison shows that the pattern remains more or less even.
These and other local freshwater studies have treated a third major zooplanktonic group, the Rotifera, with the contributions of Soto et al. (1984),
Schmid-Araya (1991), and Schmid-Araya & Zúñiga (1992). Their species
richness and seasonal variability associated with physical-chemical changes
were described. Other studies in the Antarctic Lake Kitiesh found a low zoo-
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Fig. 5. Mean species richness of total crustacean zooplankton taxa in Chilean lakes and reservoirs, separated by Copepoda and Branchiopoda. The error bars indicate standard deviations.
planktonic richness, mainly one copepod, Boeckella sp., and one anostracan,
Branchinecta gaini Daday, 1910 (cf. Montecino et al., 1991).
In search of explicatory mechanisms for the limnological patterns, an entire
line of research started around 20 years ago, mainly using mesocosm systems.
The effects of ultraviolet radiation (UV) were studied in the plankton of a high
mountain lake (Cabrera et al., 1997) and in cladocerans by Ramos-Jiliberto
et al. (2004), and on the differential tolerance of two species of crustacean
zooplankton to UV exposure by De los Ríos & Soto (2005). More recently,
Acuña et al. (2008) reported on the top-down and bottom-up regulation of
plankton biomass.
DISCUSSION
What did Bernard Dussart say about man-made lakes vs. natural lakes in
relation to key ecosystem components?
In 1984, Dussart indicated that in general, reservoirs, being recently formed,
are mostly in an early development condition or in the stage of stabilization.
Thus, organisms thriving in these man-made systems are sensitive to other environmental changes, to regular or seasonal discharges. In this sense, the water
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Fig. 6. Latitudinal distribution of crustacean zooplankton species richness in Chilean temperate
aquatic systems. For comparison, the data from Soto & Zúñiga (1991) are in bold symbols and
the present data (until 2008) in open symbols. Each symbol represents the number of species in
a different waterbody.
renewal rate is one of the important non-biological ecosystem components, as
is the shore-line development parameter (regular/irregular). Differences in the
flow of affluent streams, runoff, or seepage also affect biological activity. In
addition, mixing in man-made lakes produces a small metalimnion, though in
some reservoirs this temperature barrier can be large in summer. Wind-driven
circulation affects thermal evolution, the epilimnion accumulates heat, and the
biological activity is more intense. In general, reservoirs are sediment traps,
mostly with clear water near the dam. Also, oxygen concentration is more
spatially variable in reservoirs than in lakes, and this variability can also be
observed in the zooplankton metabolic rate studied by Andrew et al. (1989).
In continental waters, zooplankton is poorer than in the ocean, in species
number and zoological groups (Armengol, 1980), and comprises three major
groups: Protozoa, Rotifera, and Crustacea. Of these groups, Rotifera (e.g.,
Brachionus) and Anomopoda (e.g., Daphnia) with low swimming capacity
have been more successful than Copepoda. Nevertheless the higher mobility
of copepods allows them to carry out active explorations and more efficient
predation (Armengol, 1980; Kiørboe & Bagøien, 2005).
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In Chile, the maximum limnetic crustacean zooplankton species richness
found in the Araucarian Lake District region (Soto & Zúñiga, 1991), and
updated with the present information, has the same latitudinal pattern, although
the number of species sites has increased twofold (fig. 4). This is probably
a result of more intensive and extensive sampling in recent years. Additionally,
Soto & Zúñiga (1991) reported that the number of species in Chilean lakes is
much lower than in North American lakes.
The geographical distribution of zooplankton (Campos, 1984; Araya &
Zúñiga, 1985; Ruiz & Bahamonde, 1989; Soto & Zúñiga, 1991; Oyanedel
et al., 2008) shows a decrease in species richness with increasing latitude,
presumably as a consequence of Chile’s geographic isolation and species
colonization history. This decrease is attributed to a more rapid speciation
process in the Lake District region (zones WT1 and WT2), which has more
isolated drainage basins (glacial and volcanic piedmont lake formation during
the Late-Glacial and Holocene; Villagrán, 1991; Denton et al., 1999). Species
colonization is limited by the geographic and climatic features of the country
and the endemism of the calanoid copepods (Tumeodiaptomus, Boeckella,
and Parabroteas) inhabiting southern South America and Andes uplands.
This picture resembles that reported by Reid (1994) about canthocamptid
harpacticoids, which are more successful in cool humid climates of the same
region. Reid (1994) also emphasized these endemisms in relation to the
development of conservation protocols. The decline in species richness farther
south coincides with the fragmentation of the mainland at about 42◦ S (Soto
& Zúñiga, 1991), paleoclimatic features and precipitation patterns (Hulton
et al., 2002), and decreasing temperatures and productivity (Zúñiga, 1988;
Montecino, 1991).
The comparison between natural and man-made lakes, and the differential
responses for species richness observed in the present study, suggests that the
higher species diversity in Branchiopoda is associated with their shorter life
cycles and the greater environmental heterogeneity of impoundments. Gilbert
(1988) attributed the differences in the above patterns to a lower dispersal capacity (vagility) of copepods and some genera of Anomopoda, displacing protozoans and rotifers through greater competitive advantages. Larsson & Dodson (1993) reported that the production of kairomones inhibits other zooplanktonic groups, reducing species richness. In the case of total species richness of
Copepoda, this group is known to be highly dependent on water retention times
(Rocha et al., 1999). Nevertheless, compared with Brazilian impoundments
(Matsumura-Tundisi & Galizia-Tundisi, 2005), Chilean reservoirs in general
have longer water residence times.
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Why are Branchiopoda taxa important components of these temperate
lakes? The higher percentage of Branchiopoda found in the first two Chilean
hydrological-climatic zones (fig. 2) can be explained by two major factors. The
first factor is the latitudinal pattern in resources. The oligotrophy gradient starts
around 40◦ S, where the decrease of both nitrogen and phosphorus appears to
limit the growth of phytoplankton (Montecino, 1991; Steinhart et al., 1999;
Soto, 2002; Soto & De los Ríos, 2006). The second factor is the small number
of impoundments, and of reported studies in reservoirs, if any, in the extreme
southern zones.
Biogeographic studies of the conspicuous copepods Boeckella spp. indicated their broad distribution over the entire Andean range, adjacent lowlands
in Chilean and Argentinean Patagonia, and in the South Pacific islands and
Antarctica (Menu-Marque et al., 2000). In southern Chile, Villalobos et al.
(2003) found Boeckella gracilipes Daday, 1901 in lakes of Chiloé Island (4146◦ S), and, peculiarly, some marine species. In the water column, the freshwater species were concentrated mainly from 6 to 10 m depth, while the
species of marine origin were located around 10 m, since the salinity at this
depth was higher than at the surface.
It is anticipated that in the next decade, phylogenetic analysis of freshwater
organisms could help to resolve many uncertainties, as has occurred with
the genus Boeckella (cf. Adamovicz et al., 2010; Scheihing et al., 2010).
Moreover, the present picture should change significantly, as we hope to have
generated new questions about the key factors affecting zooplankton structure
and abundance.
Another area of research that should be prioritized is the characterization
and description of food webs, since this is the basis of community structure,
employing the new theoretical methodologies (i.e., modularity) coming from
other sciences such as Physics and Sociology (Bascompte, 2009). These
methods also allow us to assess the effect of disturbance at the community level
and to identify areas of conservation (Bascompte, 2007). Moreover, aquatic
food webs are now recognized to be more diverse in their carbon sources,
more complex in structure, and more versatile in their function (Reynolds,
2008). Challenges waiting to be confronted are, with priority, those related
to theoretical and applied studies about climate change, mainly related to
increases in water temperature and salinity. In the near and far future and in
consideration that the ocean and winds have a strong influence on the mixing
regimes of lakes, especially in southern Chile (Soto, 2002), rising temperatures
are likely to change the mixing depth and increase biomass and perhaps
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productivity in the lakes. It is therefore likely that the Branchiopoda could
become more prominent within the zooplanktonic communities. However,
more information and predictive models are needed to understand potential
changes in the mixing patterns. The new generation of Chilean limnologists
must face all these challenges.
In conclusion, (i) Dussart’s visit was certainly seminal to the development
of Chilean Limnology; (ii) maximum limnetic zooplankton species richness
reached in central-southern zones WT1 and WT2 also comprises a higher
percentage of Copepoda, as latitude increases; (iii) Chilean lakes are mostly
temperate with a maritime influence, favouring the overall higher species
richness of Branchiopoda with 41 species, versus 33 of Copepoda, and with
a greater presence of Branchiopoda in reservoirs; (iv) the latitudinal pattern of
higher species richness previously reported at around 40◦ S remains unaffected
by the more recent surveys.
ACKNOWLEDGEMENTS
We thank Danielle Defaye and Carel von Vaupel Klein for the invitation
to participate in this volume prepared in honour of Bernard Dussart. We
also thank Doris Soto for generous comments on this contribution, Claudio
Quezada for fig. 2, and Janet Reid for English editing.
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First received 3 May 2010.
Final version accepted 1 September 2010.