1 Internat. Rev. Hydrobiol. I 83 I 1998 I 5-6 I 439-448 I

HENDRIK SEGERS’. NINIVER L. FERRUFINO’ and LUC DE MEESTER3

’Laboratory of Animal Ecology, Zoogeography and Nature Conservation, Department Biology, University of Gent, K. L. Ledeganckstraat 35, B-9000 Gent, Belgium

’Unidad de Limnologia y Recursos Acuiticos, Universidad Mayor de San Sim6n. Casilla 5263, Cochabamba, Bolivia

’Laboratory of Ecology and Aquaculture, Katholieke Universiteit Leuven, Naamsestraat 59, B-3000 Leuven, Belgium.

Diversity and Zoogeography of Rotifera (Monogononta) in a Flood Plain Lake of the Ichilo River, Bolivia,

with Notes on Little-Known Species key words: Rotifera, taxonomy, distribution, &diversity, zoogeography

Abstract

Results are presented on a study of the momentary species diversity of Rotifera in “Laguna Bufeos”, a flood plain lake of the Ichilo River in Bolivia. A total of 104 rnorphospecies of monogonont Rotifera were identified from three samples collected on June 1, 1997. The species record includes 11 % Neotro- pica1 endemics, 5% pantropical and 13 % tropicopolitan taxa. Four taxa, viz. Aspelfa lesres HARRING and MYERS, 1928; Colurella denricuuda CARLIN, 1939; Pfygura intermedia (DAVIS, 1867) and Tricho- cerca kostei SEGERS, 1993 are newly recorded from South America, 67 morphospecies are new to the Bolivian fauna. Notes are added on some selected taxa. Brachionus amazonica KOSTE and ROBERTSON, 1983 (stat. nov.) is elevated to morphospecies rank.-

1. Introduction When compared to other South American countries, little information is available on the

Rotifera of Bolivia. Most publications that deal with the subject (ILTIS et af., 1984; PINTO, 1992; SEGERS et al., 1994; UENO, 1967), or that include notes on Bolivian Rotifera (HoL- LOWDAY and HUSSEY, 1989; KOSTE, 1977), only consider animals from the Andean part of Bolivia, and more specifically from Lake Titicaca and surroundings. There are only a few reports on the rotifer fauna of the tropical ecosystems of the country (DEL CASTILLO and MENESES, 1995; MALDONADO et al., 1996; MENESES, 1995). OLIVIER (1965) includes a few records of species inhabiting Bolivian warm waters. The dearth of information is illustrated by the fact that, prior to 1990, only some 30 rotifer species were recorded from the country (see KOSTE and JosB DE PAGGI, 1982; JosB DE PAGGI and KOSTE, 1995; DE RIDDER and SEGERS, 1997), whereas species records of over 100 taxa in single surveys of Neotropical habitats are common (see further).

The lake studied here is Laguna Bufeos, an oxbow lake in the floodplain of the Ichilo river. Several aspects of the limnology of this lake have already been studied (RF~As, 1997), or are under study, but little is known on the composition of the zooplankton community of the lake. We here present results of a study on the Rotifera of some qualitative samples, collected on the occasion of a study visit by one of us (LDM) to the region. We examine the affinities between the rotifer fauna of the lake and that of other tropical South Ameri- can lakes, and further document the distribution of Neotropical Rotifera. Taking into account that tropical floodplain lakes contain highly diverse rotifer taxocoenoses, it was, in addition, expected that a study of the rotifer constituent of the lake’s fauna would substantially add to the record of Rotifera in Bolivia.

440 H. SEGERS et ai.

COCHABAMBA 1

64O39'35" 64°40'00"

16'24'

16O27'

Map 1

2

Localisation of Laguna Bufeos.

Material and Methods

Three samples were collected on June, 1 1997 by L. DE MEESTER, using a 50 pm-mesh plankton net. Fixation was done immediately with formaldehyde (4%). Animals were picked under a WILD MI0 dissection microscope and examined and drawn using an OLYMPUS CH2 microscope with camera lu- cida. All measurements are in pm.

Laguna Bufeos (16'26's - 64.O42'E: Map 1) is an oxbow lake of the Ichilo river. It is situated at approximately 200 m a.s.1. in the province Carrasco, dept Cochabamba, Bolivia. The climate is tropi- cal, with mean annual temperature of 25 "C, and yearly precipitation of 2,OOO-2,500 mm. There is a short dry season of 1 to 4 months, during which the temperature can drop to a minimum of 14°C. Hydrologically, the system is characterized by short and irregular periods of inundation (MALDONADO et al., 1996).

3. Results and Discussion

The three samples contained a total of 104 rotifer morphospecies. One of these, a Lepa- dellu (Figs 1-2). may represent an undescribed taxon. Only a single specimen of the spe- cies was encountered, which is insufficient to warrant full description and naming of the

Diversity and Zoogeography of Rotifera in Bolivia 441

taxon. Some other animals could not be identified to species level because of taxonomic dif- ficulties. The material contained a number of taxonomically interesting morphotaxa, these are treated below. After this, the zoogeography and faunistics of the rotifer record of La- guna Bufeos is discussed.

Comments on selected taxa

Brachionidae EHRENBERG, 1938 Brachionus amazonica KOSTE and ROBERTSON, 1983 (stat. nov.)

(Figs. 3-4)

Brachionus benningi (LEISSLING, 1924) after KOSTE, 1972: see KOSTE and ROBERTSON, 1983. Brachionus urceolaris amazonica KOSTE and ROBERTSON, 1983 p. 23 I figs. 1 a-i.

Diagnosis. - Brachionus arnazonica resembles a small B. urceolaris (0. F. MULLER). The disposition of the dorsal occipital spines, lorica ornamentation, shape of foot aperture and position of the lateral antennas clearly distinguish the taxon from B. urceolaris. The species appears closely related to the Australian B. kostei SHIEL, the latter has the lateral projections of the foot aperture prolonged in acutely pointed spines.

Description. - Lorica stiff, ornamented. Lateral margins of lorica smoothly curved or angulate. Head aperture with six dorsal spines. Median and lateral pair of spines strong, intermediate pair weak. Ventral head aperture with median cavity, bordered laterally with pair of small spines. Margins, lateral of these spines sinuate. Foot aperture ventrally more deeply invaginated than dorsally, lateral projections weakly pronounced, rounded. Apertures to lateral antennas situated near the lorica margin. Trophi of the shape typical for the genus (see SEGERS er al., 1993b).

Dimensions. - Lorica length 86 (79-108), width 84 (78-83), head aperture width 73, foot aperture width 18, anterior median spine length 16, anterior intermediate spine length 3, anterior lateral spine length 12 (asexual egg 61/43) (measurements by KOSTE and ROBERTSON ( 1983) between brackets).

Comments. - KOSTE and ROBERTSON (1983) do not present their motivation for attributing subspecifc status to this taxon. Apparently, only the morphological resemblance between B. urceolaris and B. arnazonica and the fact that the latter is Neotropical motivate the sub- specific status. However, the two taxa have overlapping distributions, B. urceolaris being cosmopolitan, B. arnazonica has been recorded from Argentina, Brazil, Ecuador, Venezuela and Paraguay (see DE RIDDER and SECERS, 1997). In addition, B. arnazonica appears more closely related to a different Brachionus than B. urceolaris. These arguments argue against attributing subspecific status to the taxon. Consequently, we believe that the taxon is best treated at the morphospecies rank.

Colurellidae Colurella denticauda CARLIN, 1939

(Figs 5-6)

Colureila denticauda CARLIN, 1939 p. 12 figs 2e, h Colurella obtusa denticauda: WISZNIEWSKI (1954) p. 38 (as synonym of C. obtusa clausa HAUER, 1936)

Diagnosis. - This relatively small Colurella can be distinguished from its congeners by its elongate lorica, with nearly straight ventral and weakly curved dorsal margins, and pre- sence of two minute, acutely pointed projections on the ventro-posterior comer of the lori-

442 H. SEGERS et al.

3 4

Figures 1-2. Lepadella sp. 1 : ventral, 2: dorsal; Figs. 3-4: Brachionus ama,-onica KOSTE and ROBERTSON. 3 : ventral, 4 : dorsal; Figs. 5 -6: Colurella denricauda CARLIN, lateral; Figs. 7-8:

C. obrusa (GOSSE), lateral.

ca. Of its closest relatives, Colurellu anodontu CARLIN differs by having angulate ventro- posterior lorica corners, whereas Colurellu sinistru CARLIN has a single acutely pointed ventro-posterior projection on one side of the lorica.

Measurements. - Lorica length 50-53 (5 1 -60), lorica height 29-30 (33-39), head aper- ture height 26-27, toe length 14-18 (16-19) (measurements by CARLIN (1939) between brackets).

Distribution. - After its description from Sweden (CARLIN, 1939), the taxon has been recorded a few times from Europe only. There is a single, non-illustrated and doubtful record of C. denticuudu from North America (BERZINS, 1984). The species is new to South America.

Comments. - The synonymy of C. denticuudu with C. obtusu (GOSSE) by WISZNIEWSKI (1954, as a synonym of C. obtusu cluusa HAUER, 1936) is most likely erroneous considering the differences in lorica shape between the two taxa (compare figs. 5-6 and 7-8): C. obtusu has a less elongate lorica, with a posteriorly strongly curved dorsal margin.

Diversity and Zoogeography of Rotifera in Bolivia 443

Dicranophoridae Aspelta lestes HARRING and MYERS, 1926

Aspelta lestes HARRING and MYERS, 1926 p. 79 1-792 figs. 47 : 1-2; DE SMET (1 997) p. 1 14 figs 315-320, 16: 1-2.

Diagnosis. - This Aspelta is unmistakable by its toe shape, and, especially, by the asym- metrical, sharp alulus on the right ramus of its trophi (see DE SMET, 1997).

Distribution. - The species has to date been recorded from Europe and North America (DE SMET, 1997). It never occurs in large numbers, and its flexible lorica means that it is generally contracted and unrecognisable or passes unnoticed in preserved samples. A single specimen only was found in the present material.

Trichoceridae Trichocerca kostei SEGERS, 1993

(Figs. 9- 11)

Trichocerca kostei SEGERS, 1993 p. 59-60 figs. 24a-f.

Diagnosis. - Trichocerca kostei SEGERS is readily distinguished from other Trichocerca by its peculiar, strongly asymmetrical trophi and elongate, curved body. It can be confused with T. tigris (0. F. MULLER) (figs. 12-15), but the latter bears a large mucro dorsally on the head aperture, and its trophi have a differently shaped manubrium (T-shaped in T. tigris, L-shaped with lateral extensions in T. kostei) and left suprauncus (x in figure 9).

Distribution. - This species was described from Africa (SEGERS, 1993) and later recorded from India (SEGERS et al., 1994) and Australia (SHIEL, 1993), although the latter record may concern an undescribed relative (R. J. S H I E L , ' ~ ~ ~ ~ . comm.). The present record is the first from the New World.

Flosculariidae Ptygura intermedia (DAVIS, 1867)

Oecistes intermedius DAVIS, 1867 p. 14 figs. 1 : 5-8. Ptygura intermedia: HARRING ( 19 13) p. 89.

Diagnosis. - Ptygura intermedia is the only Ptygura that inhabits a rigid, thin-walled and dark tube, reminiscent of the tube of Limnias melicerta WEISSE, 1858. As such, it can not be confused with any congener. However, the similarity of the tube of P. intermedia with that of Limnias melicerta may cause confusion. The two taxa differ in their corona shape (rounded in Ptygura and bilobate in Limnias, although that of P. intermedia is reported rela- tively wide for a Ptygura), but also in their tube: that of P. intermedia is wider and, although the color is lighter in the basal part, a distinct smooth and hyaline basal part as in L. melicerta is not present.

Measurements. - Tube diameter basely 72-85, at 200 pm height 85-93 (for comparison: basal tube diameter 59-67, at 200 pm height 54-59 in L. melicerta; height of hyaline part of tube 46-5 1).

Distribution. - Records of P. intermedia are rare: so far, the species has been recorded from Europe and Australia only (see DE RIDDER and SEGERS, 1997). It is noteworthy that recent authors fail to record the species, which may be due to confusion with Limnias meli- certa, and to the fact that the only available figure of the taxon is the one by DAVIS (1867, reproduced in HUDSON and GOSSE (1886) and VOIGT (1957)). Our attention was only drawn

444 H. SEGERS et al.

50pm (figs 11-13) 25pm (figs 9, 10,14-15)

Figures 9-1 1. Trichocercu kostei SEGERS: 9: trophus, ventral; 10: left manubrium, lateral; 1 1 : habi- tus, lateral. Figs. 12-15: T. rigris (MULLER). 12: habitus, lateral; 13: foot and toes, ventral; 14: trophi,

ventral ; 15 : trophi, lateral.

Diversity and Zoogeography of Rotifera in Bolivia 445

to the specimens as, by coincidence, L. melicerta and P. intermedia co-occurred in one of the samples. Unfortunately, the present material concerns contracted specimens, which are unsuitable for illustrating the species. It is likely that the animal is much more widely dis- tributed than is apparent.

Species composition and zoogeography

The rotifer fauna of Laguna Bufeos as reported here consists mostly of members of Leca- ne (20%), Lepadella (13 9'0) and Trichocerca (10%). The predominance of Lecane is in agreement with reports on the rotifer fauna of other tropical floodplain lakes (e.g., Africa: SEGERS et al., 1993~; Asia: SEGERS and DE MEESTER, 1994; South America: JosE DE PAGGI, 1993). The majority of the species listed, including the Lecane and Lepadella, are littoral- periphytonic animals. The fact that these contribute most to the total species diversity is well known, and is a consequence of the weedy littoral having greater environmental heteroge- neity, allowing for finer habitat partitioning, than the pelagial (e.g., HASLER and JONES, 1949; PENNAK, 1966). The total number of species recorded is fairly high, especially considering that only three samples were available for study: in a similar survey, SEGERS and DUMONT (1996) listed 102 morphospecies from a Brazilian reservoir, whereas JosE DE PAGGI (1993) recorded the comparatively low number of 11 1 in a year-round study of an Argentinean floodplain lake, and KOSTE and ROBERTSON (1983) found 148 species in four sampling series in a Central Amazonian 'varzea' lake.

Of the 100 fully identified rotifer species recorded here, 67 are new to the Bolivian fauna, which represents a substantial addition to the Bolivian rotifer record. This is not surprising, considering that the rotifer fauna of the tropical part of the country has received little atten- tion yet, as noted above. That four species are new to South America is more noteworthy, considering the available amount of contributions relevant to the subject.

As in most rotifer surveys, the majority of' species recorded are cosmopolitan. However, a substantial number of taxa with restricted ranges are registered. Eleven taxa (1 1 %) are endemic to the Neotropical region. Some of these are widely distributed (Brachionus ama- zonica, B. mirus, B. gessneri, Lepadella donneri, Testudinella mucronata haueriensis, T. tri- dentata amazonica), Horaella thomassoni is found as far north as Mexico (RICO-MARTINEZ and SILVA-BRIANO, 1993). Others, like Floscularia armata, Lepadella amazonica, L. ne- glecta and Scaridium elongatum, are much less common. All four have only recently been described, mostly as a result of revisionary taxonomic studies, and are consequently known from a few localities only. The rate of endemicity reported here is slightly higher than that found by JosE DE PAGcr (1996) for some Argentinean subtropical waters.

One taxon, Brachionus pseudodolabratus is American, occurring in South America (Bra- zil, Venezuela, Panama, Honduras: KOSTE and JOSE DE PAGGI, 1982). and USA (Florida: AHLSTROM, 1940). Five strictly pantropical taxa are recorded. Species like Euchlanis semi- carinata, Mytilina michelangelii, Trichocerca kostei and T. voluta are rare, whereas the fact that only few records exist of F. novaezaelandiae is because the species has been overlooked in previous studies (see SEGERS et al., 1996; POURRIOT, 1996). Lepadella bicornis is known from India and South America (SEGERS et al., 1993a), but the scarcity of records indicates that it is probably premature to attribute any zoogeographical significance to this distributi- on. Thirteen taxa are tropicopolitan (Brachionus caudatus f. personatus, B. falcatus, Filinia saltator, Lecane aculeata, L. curvicornis, L. haliclysta, L. leontina, L. papuana, L. rhytida, L. signifera, L. undulata, Lepadella costatoides, Platyias leloupi). The remaining taxa are either cosmopolitan or have insufficiently documented ranges.

446 H. SEGERS et al.

Table 1. Rotifer species record in Laguna Bufeo, 1 June 1997. *: new to Bolivia; **: new to South America.

*Anuraeopsis jissa (GOSSE, 185 1 ) *Ascomorpha ecaudis PERTY, 1850 **Aspelta testes HARRING and MYERS, 1928 Asplanchna sieboldi (LEYDIG, 1854) *Brachionus amazonica KOSTE and ROBERTSON,

I983 (stat. nov.) B. caudatus BARROIS and DADAY, 1894 f. perso-

natus AHLSTROM, 1940 B. falcatus ZACHARIAS, I898 *B. pseudodolabratus AHLSTROM, 1940 B. quadridentatus (HERMANN, 1783) f. melheni

*B. voigti HAUER, 1961 B. zahniseri AHLSTROM, I934 f. gessneri HAUER,

*Cephalodella forficula (EHRENBERG, 1832) C. gibba (EHRENBERG, 1832) *C. sterea (GOSSE, 1887) *Cnlurella colurus (EHRENBERG, 1830) **C. denricauda CARLIN, 1939 C. obrusa (Gosse, 1886) C. uncinata (0. F. MULLER, 1773) f. bicuspidara

(EHRENBERG, 1832) *Conochilus cf. coenobasis SKORIKOV, 19 14 Dicranophorus epicharis HARRING and MYERS,

1928 *D. grandis (EHRENBERG, 1832) *D. luetkeni (BERGENDAL, 1892) *D. prionacis HARRING and MYERS, 1928 *Dipleuchlanis propatula (GOSSE, 1886) Euchlanis dilatata (EHRENBERG, 1832) *E. incisa CARLIN, 1939 *E. semicarinata SEGERS, 1993 *Filinia novaezealandiae SHIEL and SANO-

*F. saltator (Goss~, 1886) *Floscularia armata SEGERS, 1997 *F. conifera (HUDSON, 1881) *Hexartha mira (HUDSON, 1871) *floraella thomassoni KOSTE, 1973 Lecane aculeara (JAKUBSKI, 1912) *L. bifurca (BRYCE, 1892) L. bulla (Goss~, 185 I )

L. closterocerca (SCHMARDA, 1859) L. cornuta (MULLER, 1886) L. curvicomis (MURRAY, 1913) L. elsa HAUER, 1931 *L furcata (MURRAY, 1913) *L haliclysta HARRING and MYERS, 1926 L. hamata (STOKES. 1896) *L. inermis (BRYCE, 1892) L. leontina (TURNER, 1892) *L ludwigii (ECKSTEIN, 1883) f . typica

L. lunaris (EHRENBERG, 1832) L. papuana (MURRAY, 1913) L. quadridentata (EHRENBERG, 1832)

BARROIS and DADAY, 1894

1956

AMUANG, 1993

f. fypica f. goniata (HARRING and MYERS, 1926)

f . ohioensis (HERRICK, 1885)

*L. rhytida HARRING and MYERS, 1926 L. signifera (JENNINGS, 1896) f. ploenensis

*L. undulata HAUER, 1938 L. ungulata (Goss~, 1887) Lepadelia amazonica SEGERS, 1993 *L. apsida HARRING, 1916 *L benjamini HARRING, 19 16 *L. costatoides SEGERS, 1992 *L. dactyliseta (STENROOS, 1898) L. donneri KOSTE, 1972 *L. minuta (WEBER and MONTET, 1918) *L. neglecfa SEGERS and DUMONT, 1995 L. uvulis (M~LLER, 1786) *L. ruttenburgi (LUCKS, 19 12) Lepadella species *L. triba MYERS, 1934 *L. bicornis VASISHT and B A ~ I S H , 197 1 *Limnias ceratophylli SCHRANK, 1803 *L melicerta WEissE, 1848 *Macrochaetus collinsi (GOSSE, 1867) *Monommata grandis TESSIN, 1890 *Mytiha bisulcata (LUCKS, 19 12) *M. michelangellii REID and TURNER, 1988 M. ventralis (EHRENBERG, 1832) *N. cf. pachyura (GOSSE, 1886) *Norornmata saccigera EHRENBERG, 1832 Notommata species Plationus patulus (MULLER) f. typica

f. macracanthus (DADAY, 1905) Platyias leloupi GILLARD, 1957 P. quadricomis (EHRENBERG, 1832) *Polyarthra longiremis CARLIN, 1943 P. spec. near vulgaris (sensu SEGERS and

P. cf. vulgaris CARLIN, 1943 *Proales fallaciosa WULFERT, 1937 **Ptygura intermedia (DAVIS, 1867) *Scaridium bostjani DAEMS and DUMONT, 1974 *S. elongatum SEGERS, 1996 *Sinantherinn ariprepes EDMONDSON, 1939 *Synchaeta longipes GOSSE, 1887 *S. pectinata EHRENBERG, 1832 *Testudinella emarginula (STENROOS, 1898) *T. mucronata haueriensis GILLARD, 1967 T. patina (HERMANN, 1783) *T. tridentata amazonica THOMASSON, 197 1 Trichocerca bicristata (Goss~, 1887) *T. bidens (LUCKS, 1912) *T. bruchyura (GOSSE, 1851) T. brazifiensis (MURRAY, 1913) **T. kostei SEGERS, 1993

*T. sirnilis (WIERZEJSKI, 1893) *T. tenuior (GOSSE, 1886) *T. tigris (MULLER, 1786) *T. volutu (MURRAY, 1913) *Trichotria tetractis (EHRENBERG, 1830)

(VOIGT, 1902)

DUMONT, 1996)

*T. pusilla (JENNINGS, 1903)

Diversity and Zoogeography of Rotifera in Bolivia 447

4. Conclusions

The results of this survey include the addition of four species to the South American, and 67 to the Bolivian rotifer fauna, of a total of 100 fully identified morphospecies. This indi- cates that, whereas the Rotifera of tropical South America as a whole is quite well-docu- mented, this is not the case for Bolivia. The rotifer taxocoenosis of the studied lake pre- dominantly consists of littoral taxa, exemplified by a high proportion of Lecane. Eleven percent of the rotifers are Neotropical endemics, 5 % are pantropical, 13 % are tropicopolitan. The studied lake had a relatively high a-diversity of Rotifera at the time of sampling, espe- cially considering the limited number of samples available for study.

5 . Acknowledgements

Samples for this study were collected during a visit of LDM to Laguna Bufeos, sponsored by the VL.1.R. project “Limnological studies” in the Department of Cochabamba (PROLIMCO).

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ski Arch. Hydr. 2/15: 7-249.

Manuscript received May 4th, 1998; revised July 6th. 1998; accepted July 14th. 1998