1
Vertical distribution of two morphoptypes of the rotifer
Brachionus havanaensis (Stemberger, 1979) in a shallow lake
Paula V. Weigand1, 2 & Alicia H. Escalante1, 2
1
Laboratorio de Limnología, Departamento de Biología, Facultad de Ciencias Exactas y
Naturales, Universidad Nacional de Mar del Plata, Funes 3250 – 3º Piso – 7600 Mar del Plata,
Argentina
2
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).
(pweigand@mdp.edu.ar/aescalan@mdp.edu.ar)
2
ABSTRACT. During summer 2002 the zooplankton community of Lake Los Padres
(Argentina) was numerically dominated by rotifers, especially Brachionus havanaensis
(Stemberger, 1979), B. caudatus (Barrois & Daday, 1894), B. calyciflorus (Pallas, 1766),
Filinia longiseta (Ehrenberg, 1834), Keratella quadrata (O.F. Muller, 1786) and K.
americana (Carlin, 1943). Given that Brachionus havanaensis is one of the most common
herbivorous species in the zooplankton from tropical and subtropical America, the aim of this
work was to study its vertical distribution and to look for the existence of more than one
morphotype of the species. Two morphos of B. havanaensis were found in the water column
from the pelagic zone during the time of sampling. Changes in shape in B. havanaensis
individuals with cyclomorphosis involved a larger body size and longer occipital and caudal
spines than those from non-cyclomorphic individuals. As far as we are concerned, the small
differences observed in the diel vertical distribution of the two B. havanaensis morphotypes
are not enough to conclude that they vertically migrate, particularly in a shallow lake, where
wind can mix the whole water column. Through this research we were able to identify and
describe for the first time two summer morphotypes of B. havanaensis and their vertical
distribution in a shallow, eutrophic and non-stratified lake.
Keywords: vertical distribution, cyclomorphosis, shallow lake, Brachionus havanaensis.
RESUMEN. Durante el verano de 2002 la comunidad zooplanctónica de la Laguna de Los
Padres (Argentina) estuvo dominada por rotíferos, especialmente Brachionus havanaensis
(Stemberger, 1979), B. caudatus (Barrois & Daday, 1894), B. calyciflorus (Pallas, 1766),
Filinia longiseta (Ehrenberg, 1834), Keratella quadrata (O.F. Muller, 1786) and K.
americana (Carlin, 1943). Dado que B. havanaensis es una de las especies herbívoras más
comunes del zooplancton de América tropical y subtropical, el objetivo de este trabajo fue
estudiar su distribución vertical y verificar la existencia de más de un morfotipo de la especie.
Durante el muestreo se hallaron dos morfos de B. havanaensis en la columna de agua de la
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zona pelágica. Los individuos de B. havanaensis con ciclomorfosis presentaron mayor tamaño
corporal y espinas occipitales y caudales más largas que los individuos sin ciclomorfosis. Las
pequeñas diferencias observadas en la distribución vertical diaria de los dos morfotipos de B.
havanaensis no son suficientes para concluir que migran verticalmente, particularmente en un
lago de escasa profundidad como Los Padres, donde el viento alcanza a mezclar
completamente la columna de agua. A través de esta investigación se pudieron identificar y
describir por primera vez dos morfotipos de B. havanaensis y su distribución vertical en un
lago somero, eutrófico y no estratificado.
Palabras clave: distribución vertical, ciclomorfosis, lago somero, Brachionus havanaensis.
4
INTRODUCTION
Description of the community structure and spatial variation are usually some of the main
objectives of researches on zooplankton ecology (PINEL-ALLOUL, 1995). Several studies have
suggested the important influence of different factors determining the distribution and
abundance of zooplankton in freshwater bodies. Among the abiotic variables, temperature and
pH play an important role (HUTCHINSON, 1967) while among the biotic interactions food
availability and predation are the major forces influencing the abundance of zooplankton
(LAMPERT & SOMMER, 1997).
Among small aquatic organisms, different morphotypes of a single species can vary
seasonally in successive generations. This phenomenon is called cyclomorphosis or seasonal
polymorphism, being conspicuous among planktonic cladocerans (JACOBS, 1980; HAVEL,
1985; YURISTA, 2000), and fairly common in rotifers (GILBERT & WAAGE, 1967; GILBERT &
STEMBERGER, 1984). The most noticeable cyclomorphosis involves the development of body
processes and/or spines and other outgrowths of the body wall (HUTCHINSON, 1967;
MARGALEF, 1983) which can be controlled by temperature, food quantity or quality, predator
kairomones (GILBERT & WAAGE, 1967; GILBERT, 1999; SARMA et al., 2003), turbulence and
viscosity (KERFOOT, 1980). Earlier investigations have assumed that cyclomorphic individuals
would have greater resistance to sink because water viscosity decreases at high temperature
(WETZEL, 2001).
In some ecosystems, the zooplankton populations daily exhibit different vertical
distribution. This movement, called vertical migration, varies from few centimeters to several
tens of meters in lakes, or even hundreds of meters in the open ocean (HUTCHINSON, 1967; DE
MEESTER et al., 1999). Vertical distribution can vary not only among species, but within one
species as well (FORWARD, 1988; SEKINO & YAMAMURA, 1999).
Rotifers are important members of the zooplankton, and may contribute a significant
proportion of the zooplankton biomass and community grazing rate (PACE & ORCUTT, 1981).
5
Nevertheless, the occurrence of cyclomorphosis and the vertical distribution of rotifers
inhabiting Pampasic lakes from Buenos Aires province are still unknown. Given that
Brachionus havanaensis (Stemberger, 1979) is one of the most common herbivorous species
in the zooplankton from tropical and subtropical America, the aim of this work was to study
its vertical distribution and to look for the existence of more than one morphotype of B.
havanaensis living together during summer in Lake Los Padres, Argentina.
MATERIALS AND METHODS
Lake Los Padres (Fig. 1) is a shallow eutrophic lake located at the eastern border of Sierra
de Los Padres, in Buenos Aires province, Argentina (37º 56' 30” S, 57º 44' 30” W). Its surface
area is 2.16 km2, with a mean depth of 1.24 m (POZZOBON & TELL, 1995). It can be classified
as a polymictic lake because of the lack of thermal stratification.
Replicated samples of zooplankton were taken in the pelagic zone during summer 2002: at
midday, before and after sunset, at midnight and before and after sunrise, using the 12 L
Schindler-Patalas plankton trap with a 30 µm mesh net (SCHINDLER, 1969). Samples for
qualitative and quantitative analysis were collected every 0.30 m, including the whole vertical
profile up to 2.10 m. Zooplankton qualitative samples were maintained alive and used for
species identification, while the quantitative ones were fixed prior carrying them to the
laboratory.
Depth of water column, water transparency (Secchi disk), water temperature and pH were
in situ recorded at each sampling time.
Maximum body length and width, and occipital and caudal spine lengths of cyclomorphic
and non-cyclomorphic individuals of Brachionus havanaensis were measured. A one way
analysis of variance was used to test normality of data. A statistical non-parametric one way
analysis of variance on ranks Kruskal-Wallis test was performed in order to locate significant
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differences in body size among individuals of the same B. havanaensis morph along the water
column (ZAR, 1984).
Previously to counting, samples were homogenized using a magnetic stirrer HI 190M.
Counts were performed in a 1 mL Sedgwick-Rafter chamber under an Olympus CH30
microscope. Brachionus havanaensis abundance was expressed as the number of individuals
per litre (ind L-1) (JOSÉ DE PAGGI & PAGGI, 1995).
The Chi-square (²) test was performed in order to locate significant differences in the
vertical distribution of B. havanaensis individuals along the water column for each depth and
each time of sampling (Zar, 1984).
Berger-Parker dominance index (DI) (Moreno, 2001) was used for each time and each
depth of sampling, indicated as:
DI = N¡ max / N¡
where N¡ max indicates the number of individuals of the dominant morph in the ¡th stratum
and N¡ is the total number of B. havanaensis individuals in the ¡th stratum.
From data of abundance, mean depth (MD) was calculated as:
MD = Σ (N¡ x d¡) / Σ N¡
where N¡ is the concentration of B. havanaensis individuals at ¡ depth and d¡ is the depth of
the ¡th sample (BOLLENS & FROST, 1992; DE STASIO, 1993). The amplitude refers to the extent
of diel oscillation of the MD, computed by subtraction of the maximum and minimum values
of the MD obtained along the diel cycle (DODSON, 1990; BOLLENS & FROST, 1992; RODRIGO
et al., 1999; ARMENGOL & MIRACLE, 2000).
RESULTS
At the time of this study, zooplankton community of Lake Los Padres was numerically
dominated by rotifers, especially Brachionus havanaensis, B. caudatus (Barrois & Daday,
1894), B. calyciflorus (Pallas, 1766), Filinia longiseta (Ehrenberg, 1834), Keratella quadrata
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(O.F. Muller, 1786) and K. americana (Carlin, 1943). When sampling the day with the
highest mean water temperature, two morphotypes of B. havanaensis were found. The same
day Lake Los Padres showed a water transparency value of 0.35 m and an alkaline pH, with a
mean value of 8.6. Mean water temperature values from different depths showed no
differences between day and night (light: 20.7 º C / dark: 20.0 º C).
These two morphotypes differed in the occipital and caudal spine lengths and in body size
(Fig. 2; Table I). Individuals of each morph showed no statistically significant differences in
body size along the water column (cyclomorphic p= 0.079; non-cyclomorphic p= 0.166).
Brachionus havanaensis was the dominant species among rotifers along the water column
(DI: 0.92 ± 0.01).The highest density of cyclomorphic individuals was 1236 ± 132 ind L-1 at
midnight between 0.90 and 1.20 m (Fig. 3-A) and that of non-cyclomorphic individuals was
7432 ± 488 ind L-1 at the same time and depth than those of cyclomorphic individuals (Fig. 3B).
Non-cyclomorphic and cyclomorphic individuals of B. havanaensis were found along the
vertical profile throughout the whole diel cycle, with statistically significant differences of
distribution at different sampling times (², p < 0.05).
The greatest value of MD for short-spined B. havanaensis (non-cyclomorphic) individuals
was after sunrise and the least one after sunset, with an amplitude of 0.29 ± 0.02 m. On the
contrary, maximum MD for cyclomorphic or long-spined individuals was after sunset and the
minimum value before sunset (0.23 ± 0.03 m) (Fig. 4).
DISCUSSION
The zooplankton community from Los Padres Lake was dominated by rotifers, as
commonly occurs in eutrophic environments (RAVERA, 1996). Brachionus havanaensis was
the most abundant species among summer rotifer plankton, and two morphotypes of this
species were found along the whole water column.
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The most common changes among some rotifer species include an increase in body size,
and the appearance and/or elongation of spines (WETZEL, 2001). In this study, spine induction
in B. havanaensis was observed. This could be determined by temperature as it was observed
in other rotifer species (CONDE-PORCUNA & DECLERK, 1998). We could not predict that the
polymorphism observed could be induced by predators, as it was observed by other authors
(GILBERT, 1999; GILBERT & STEMBERGER, 1984; SARMA et al., 2003), because during the time
of sampling no B. havanaensis predator was detected.
The vertical distribution of zooplankton is of great ecological complexity since it is related
to various environmental factors. In well stratified lakes it is common to observe diel vertical
migration (MARGALEF, 1983). ARMENGOL & MIRACLE (2000) mentioned the simultaneous
presence of several Keratella quadrata morphs with different vertical distribution along the
water column in Lake La Cruz, Spain. The migratory behavior of rotifer species in different
lakes from Argentina is mainly related to lake trophic status, resources availability and water
temperature (DIPPOLITO, 1988; GABELLONE et al., 2000). Among rotifers from a Paraná River
floodplain lake, different patterns of vertical migration were observed (JOSÉ DE PAGGI, 1995).
This author showed that some species migrate upwards during the day while others swim
downwards, suggesting that rotifers do not show an evident pattern of vertical migration in
shallow lakes.
But in Los Padres Lake, a shallow one, the small differences in the vertical distribution are
not enough to conclude that there is a vertical migration of the rotifer species under study,
given that wind can mix the whole water column. Among several factors that could have been
affecting the vertical distribution, fish predation was excluded in this case due to the mortality
observed few months before sampling.
Through this research we were able to identify and describe for the first time two summer
morphotypes of B. havanaensis and their vertical distribution in a shallow eutrophic lake.
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Future studies will be necessary to determine which environmental factors control the
development of polymorphism and to demonstrate the phenotypic plasticity of this species.
Furthermore, detailed researches should be necessary to find out if the different number of
individuals observed in the water column is due only to vertical but to horizontal variation as
well.
Acknowledgements. Financial support was provided from an EXA grant (National
University of Mar del Plata (UNMdP, Argentina) to A.H.E. We also thank H. Vittorio for his
help in the field, A. Licciardo for her technical support in the field and the laboratory, Dr. J.J.
Gilbert and Dr. Ing. Agr. G.A. Studdert for the revision of a previous version of the
manuscript. We thank the Histology and Histochemistry Laboratory (UNMdP) for allowing
us to take the photographs.
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Table I. Biometrical comparisons between two morphotypes of Brachionus havanaensis
(Stemberger, 1979) from Lake Los Padres, Argentina.
A, total length; B, body length; C, body width; D, occipital spine length; E, caudal spine
length. Measurements in µm ± SD.
A
B. havanaensis
(cyclomorphic)
365,9 ± 7,9
B. havanaensis
(non-cyclomorphic) 284,2 ± 27,6
B
C
D
E
118,5 ± 2,9
59,2 ± 2,1
159,1 ± 7,4
147,66 ± 3,2
98,9 ± 9,4
49,9 ± 5,2
114,4 ± 14,6
119,9 ± 8,9
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FIGURE LEGENDS
Fig. 1. Map of Lake Los Padres, Argentina. Study site ( • ).
Fig. 2. Photographs of cyclomorphic (A) and non-cyclomorphic (B) Brachionus havanaensis
individuals from Lake Los Padres, Argentina.
Fig. 3. Vertical profiles of cyclomorphic (A) and non-cyclomorphic (B) Brachionus
havanaensis individuals. Histograms show the abundance (Log ind L-1 ± SD) at each stratum,
the solid vertical line indicates the tendency. Times of sampling indicated as: MD, midday;
BSS, before sunset; ASS, after sunset; MN, midnight; BSR, before sunrise; ASR, after
sunrise. Depths indicated as: 1, 0-0.30 m; 2, 0.30-0.60 m; 3, 0.60-0.90 m; 4, 0.90-1.20 m; 5,
1.20-1.50 m; 6, 1.50-1.80 m and 7, 1.80-2.10 m.
Fig. 4. Mean depth (MD) ± SD values of the two morphotypes of Brachionus havanaensis.
Times of sampling indicated as: MD, midday; BSS, before sunset; ASS, after sunset; MN,
midnight; BSR, before sunrise; ASR, after sunrise. (□) indicates cyclomorphic individuals and
(♦) indicates non-cyclomorphic individuals.