Separation of two Neotropical species: Macrothrix superaculeata (Smirnov, 1982) versus M. elegans Sars, 1901 (Macrothricidae, Anomopoda, Cladocera)

Hydrobiologia 517: 61–88, 2004. © 2004 Kluwer Academic Publishers. Printed in the Netherlands.

61

Separation of two Neotropical species: Macrothrix superaculeata (Smirnov, 1982) versus M. elegans Sars, 1901 (Macrothricidae, Anomopoda, Cladocera) Alexey A. Kotov1,2, Tania Garfias-Espejo2 & Manuel El´ıas-Guti´errez2∗ 1 A.

N. Severtsov Institute of Ecology and Evolution, Leninsky Prospect 33, Moscow 117071, Russia E-mail: [email protected] 2 El Colegio de la Frontera Sur, Av. Centenario Km 5.5, Chetumal 77900, Quintana Roo, Mexico E-mail: [email protected] ∗ Author for correspondence Received 1 February 2003; in revised form 12 September 2003; accepted 18 September 2003

Key words: taxonomy, neotropics, morphology, macrotricid, morphological variability

Abstract The morphology of two Neotropical taxa, Macrothrix elegans Sars, 1901 and M. superaculeata (Smirnov, 1982) (Macrothricidae, Anomopoda, Cladocera) was redescribed, based on type materials (a lectotype of M. elegans was selected here), and additional samples from the Americas. Previous conclusion about synonymy of both species was erroneous, because it was based on limited material from South America. M. superaculeata differs from M. elegans in the presence of a sharp spine at postero-dorsal angle of valves; a more fine ring around dorsal head pore; thinner hexagonal reticulation of valves; the presence of setules on basal segment of postabdominal seta; armature of exopod on antenna II, and some features of thoracic limbs. Previously, the discriminative features of the two species were not formulated accurately, and it was a reason of several misidentifications. Actually, M. superaculeata is found only in a limited set of localities from the Amazon basin, while M. elegans is one of the most common anomopod species in all Neotropics, from Argentina to Mexico. Abbreviations: Collections: AAK, personal collection of A. A. Kotov, Moscow, Russia; ECO-CH-ZOO, zoological collection of El Colegio de la Frontera Sur, Chetumal, Mexico; GOS, collection of G. O. Sars, Zoological Museum of the Oslo University, Norway; MGU, Zoological Museum of Moscow State University; NHM, the Natural History Museum, London, United Kingdom; NNS, collection of Prof. N. N. Smirnov, now keeping at the Zoological Museum of Moscow State University, but not officially deposited to it; ZIN, Zoological Institute of Russian Academy of Sciences, St. Petersburg, Russia. Collectors: AAK, A. A. Kotov; ACM, A. Cervantes-Mart´ınez; AGM, A. E. Garc´ıa-Morales; GOB, G.-O. Brandorff; J GRK, J. G. Granados-Ram´ırez; ICO, I. Castellanos-Osorio; MAG, M. A. Gololobova; MGA, M. Guti´errez-Aguirre; MEG, M. El´ıas-Guti´errez; NNS, N. N. Smirnov; nd, no data on collector or date of sampling. In text and pictures: IDL, inner distal lobe of limb I; mxI, maxilla I; mxII, maxilla II; ODL, outer distal lobe of limb I; pgn, paragnaths. Introduction Smirnov (1992) suggested that ‘Macrothrix triserialis Brady, 1886’ is a complex of close congeners. Recently Dumont et al. (2002) revised the systematics of Macrothrix rosea-triserialis species group (Macro-

thricidae, Anomopoda, Cladocera), based in detailed analysis of the morphology of several populations from different continents, demonstrated that there are regional differences between them, mainly in the thoracic limb structure. But there are some taxonomical inconsistencies in this, excellent in the part of

62 morphology, article. Some earlier described taxa, i.e. M. chevreuxi Guerne & Richard, 1892 from Africa and M. shadini Mukhamediev, 1963 from Middle Asia, which are surely triserialis-like (Harding, 1955; Smirnov, 1976, 1992), retained without author’s attention. Also Dumont et al. (2002) examined only a single species from South America, which was named M. elegans Sars, 1901, while M. superaculeata (Smirnov, 1982) was reported as a junior synonym of the former. But this conclusion was based on analysis of a single population from Broa (Brazil), without a evaluation of inter-population variability and a re-examination of type materials of both species, which are accessible. In this article we re-describe M. elegans and M. superaculeata based on type materials of Sars and Smirnov. Also, we examined morphology and variability of a row of populations from Brazil and other localities of South, Central and North America with the aim to determine how many trisertialis-like species are in Neotropics.

postabdomen preanal margin; SS, length of second segment of antennal exopod; MS, length of main (true) spine on second exopod segment; AD1, AD2, length of first and second additional spine on second exopod segment. Then, some ratios were calculated for each animal, after that, averages and ranges were determined for each population. Ranges are represented in Table 2. Averages of BH/BL, PO/BL, PP/BL, PP/PO, TOO/BL, MS/SS, AD1/SS, AD2/SS, AD1/MS and AD1/AD2 for each population were incorporated into a cluster analysis by using as a distance measure the Euclidean Distance and unweighted pair-group average as a linkage rule, to determine differences among populations. Finally, a discriminant function analysis to the same ratios (except PP/B2) was performed. After a test with a normal probability plot, we used a natural logarithm transformation of data PP/PO, AD1/SS, and AD1/AD2 in order to adjust their distributions. All statistical analyses were performed with Statistica release 4.3 software.

Material and methods

Results

Animals were selected from preserved samples under a binocular stereoscopic microscope, placed on slides (in a drop of a glycerol-formaldehyde mixture) and studied under an optical microscope in toto. At least three parthenogenetic females from each locality (with the exception of the museum loans) were dissected under a stereoscopic microscope for the study of appendages and postabdomen. A single female was dissected from Sars’s type material, with permission of the Collection Manager. The parts from dissection were kept on a series of slides like a single paralectotype (Table 1). Drawings were prepared by using a camera lucida attached to an Alphaphot compound microscope. A system of numeration for different setae on thoracic limbs proposed by Kotov (2000, 2003) for chydorids was used here also, on basis of the similarity of limbs in Chydoridae and Macrothricidae (Smirnov, 1969, 1971; Dumont & Silva-Briano, 1998). All operations with SEM were conducted like in previous cases (Kotov, 2000, 2003). In order to establish if exists morphometric differences between M. elegans and M. superaculeata, the following measurements were made for 10 parthenogenetic females of maximum size for a population: BL, body length; BH, body height; PO, pore size; PP, postpore distance; TO, length of largest tooth on

Macrothrix elegans Sars, 1901 Sars, 1901: 33–36, pl. 6: Figs 1–9; Daday, 1905: 194; Stingelin, 1913: 615–616, Figs 18– 19 (triserialis var. chevreuxi); Delachaux, 1919: 25–26 (triserialis var. chevreuxi); Brehm & Thomsen, 1936: 213 (triserialis); Brehm, 1937: 498 (triserialis); 1938: (tenuicornis var. maxima);1939: 181 (triserialis); Harding, 1955: 338–339, Figs 34– 36 (triserialis); Orghidan & Negrea, 1973: 107–109, Fig. 3 (triserialis); Van de Velde et al., 1978: 394 (triserialis); Infante, 1980: 597–598, Fig. 4 (Echinisca triserialis); Frey, 1982: 179 (elegans and triserialis); Montú & Gloeden, 1986: 31, Figs 8c–f; Valdivia Villar, 1988: 293 (Echinisca triserialis); Smirnov, 1992: 51, 53, 74, 76–80 (triserialis from South America and superaculeata from Xingú, Lago Grande and Santa Fe); Paggi, 1995: Figs 94–97 (Echinisca); Ciros-Pérez & Elías-Gutiérrez, 1996: 298, Figs 1–2 (triserialis); Elmoor-Loureiro, 1998: 25 (triserialis); Dumont et al., 2002: 8, Figs 65–76 (elegans); 8–9, Figs 77–88 (cf. triserialis from Mexico). Type locality: Itatiba, State of São Paulo, Brazil (according to lectotype). Before this moment, it was not specified accurately, the species was obtained from dried mud from 4 different localities, reported by Sars (1901) approximately: ‘São Paulo, Itatiba, Ipiranga,

63 Table 1. Lectotype and paralectotypes of Macrothrix elegans Sars, 1901 selected here. Status

Museum

Inventory number

Type

Locality

Number of specimens

Sex

Lectotype Paralectotypes Paralectotypes Paralectotype Paralectotypes Paralectotypes Paralectotypes Paralectotypes

GOS GOS GOS GOS GOS GOS NHM NHM

F 18448a F 18448b F 18448c-d F 23218 F 18447 F 18449 1901.12.12.208 1901.12.12.208–211

Tube Tube Slide Tube Tube Tube Slide Tube

Itatiba Itatiba Itatiba São Paulo São Paulo Argentina Argentina Argentina

1 226 1 1 19 387 2 126

Parth. ♀ Parth. ♀♀ Parth. ♀, dissected ♂ Parth. ♀♀ & ♂♂ Parth., eph. ♀♀ & ♂♂ Parth. ♀♀ Parth. ♀♀

and Argentina’ (all three Brazilian localities are in the State of São Paulo, more or less closely located, no idea about the site in Argentina). Lectotype and paralecotypes (selected here): see Table 1. Other material examined: Argentina. Santa Fe: backwaters and tributaries of Rio Santa Fe, and ditches, pools and puddles in the region of Santa Fe city, NNS-1997-025-028, -044, -090, -177, -239, NNS-1999-076-079 (all samples were collected 2.05–09.07.1981 by NNS). Brazil. São Paulo: Broa Res. (22◦ 10 S, 47◦ 54 W), 300 km inland from Atlantic coast, coll. 19.01.1996 by H. Segers, NNS-1997-260; NNS-1997-273. Maranhao: ephemeral dune pools in Lençóis Maranhenses dune field (02◦ 35 50 S, 42◦ 42 46 W), coll. 24.12.1997 by K. Van Damme, AAK2002-006; Mato Grosso do Sul: Baia do Castelo, N of Corumbá, Pantanal, coll. 23.04.1998 by GOB, AAK-1998057. Amazonas: Lago Grande, Amazon basin, coll. 10.04.1983 by M. V. Mina, AAK2002-020; Ilha do Muratú, coll. 07.05.1975 by GOB, AAK-1999-057; Pará: Rio Arapiuns, tributary of Rio Tapajós, coll. 04.12.1996 by GOB, AAK–2002-021; Rio CeraímaMirim, coll. by GOB (completely dissected and not saved). Bolivia. Inundated meadow with Utricularia near Laguna Prado de Riberalta, coll. 25.09.1975 by GOB, AAK-1999-060. Nicaragua. Open littoral, bays and tributaries of Nicaragua lake (Cocibolca), coll. 14.02.1985 and 24.05.1985, NNS-1997-023, -034, -174, NNS-1999020, -030, NNS-2000-005; Rio Limon at Lago de Nicaragua, coll. 24.05.1988; Rio Majastre at Nicaragua lake, coll. 24.05.1988, NNS-1997-023; a

rice field near Tisma, coll. 25.05.1988, NNS-1997020; Rio Tipitapa, its backwaters and pools and a canal near it, coll. 17.05.1988, NNS-1997-021, -1997-252, 1998-161; pond at Institute de los Recursos Naturales, Managua, coll. 27.01.85 (all samples were collected by NNS). Guatemala. Alta Verapaz: small ponds 5 km from Raxruja (15◦ 49 26 N, 89◦ 57 20 W), coll. 09.04.2002 by MEG, AAK & MAG; a pond, also near Raxruja (15◦ 51 50.7 N, 90◦ 01 01.9 W), coll. 18.05.2001 by MEG; a pond near San Antonio Flores (15◦ 49 26 N, 89◦ 57 20 W), coll. 09.04.2002 by MEG, AAK & MAG; a small flow near Chajmaic bridge (15◦ 43 15 N, 89◦ 56 24 W), coll. 24.03.2000 by MEG; a permanent lagoon with Nymphaea (15◦ 58 53 N, 90◦ 26 33 W), coll. 06.04.2002 by MEG, AAK & MAG. Petén Flores: series of samples in shore zone of lake Petén (16◦ 55 N, 89◦ 53 W; 16◦ 55 44 N, 89◦ 53 38 W; 16◦ 55 35 N, 89◦ 55 30 W; 16◦ 55 30 N, 89◦ 51 27 W; 16◦ 59 34 N, 89◦ 41 39 W; 16◦ 56 00 N, 89◦ 53 22 W), coll. 05.07. 1999 by MEG and 09.04.2002 by MEG & AAK; a puddle near Sayanche (16◦ 26 49.9 N, 90◦ 07 08.6 ), coll. 18.05.2001 by MEG; a pond near El Pato crossing roads (16◦ 03 37.5 N, 90◦ 10 51.2 W), coll. 18.05.01 by MEG; a small lagoon near lake Petén (16◦ 54 13 N, 89◦ 46 36 W), coll. 21.03.2000 by MEG; flooded wetland near Melchor de Mencos (17◦ 01 37.4 N, 89◦ 14 08.8 W), coll. 19.05.2001 by MEG. Belize. A small puddle near Spanish Lockout (17◦ 13 54.1 N, 88◦ 55 49.2 W), coll. 16.06.2001 by MEG, AAK & AGM; a small puddle near La Democracia (17◦ 21 53.9 N, 88◦ 32 20.7 W), coll. 06.09.1997 by MEG, AAK & AGM; a small

64

Figures 1–12. Macrothrix elegans, parthenogenetic females from culture of G. O. Sars, hatched from mud collected from unknown water body in Itatiba, São Paulo State (1–2, lectotype; 7–12, paralectotype), and Baia do Castelo, N of Corumb´a, Mato Grosso do Sul, Brazil, coll. 23.04.1998 by G.-O. Brandorff (3-6): Figures 1, 2, lectotype in lateral and anterior view; Figs 3, 5, adult in lateral and dorsal view; Fig. 4, juvenile; Figs 6, 7, head and dorsal head pore; Fig. 8, labrum and antenna I; Fig. 9, dorsal margin of valves; Figs 10–12, setules at anterior, medium and posterior portion of ventral margin. Scale bar denotes 100 µm.

puddle near Zoological garden (17◦ 24 23 N, 88◦ 24 00 W), coll. 06.09.1997 by MEG. Mexico. Quintana Roo State: two unnamed lagoons and a channel to Rio Hondo near Subteniente López village (18◦ 30 03 N, 88◦ 23 25 W; 18◦ 29 49 N, 88◦ 21 01 W and 18◦ 29 54 N, 88◦ 23 28 W), coll. 29.09.1998 by NNS & MEG; a temporary puddle in Huay-pix village (18◦ 30 N, 88◦ 26 W), coll. 25.06.1995, nd; a small river near Puente Milagros (18◦ 31 N, 88◦ 23 W), nd, nd; three pools near Tres

Ríos, vicinity of Chetumal town (18◦ 31 37.4 N, 88◦ 22 43.6 W; 18◦ 34 37 N, 88◦ 25 04.5 W and 18◦ 34 33.6 N, 88◦ 24 53.6 W); different localities in shore zone of Bacalar lagoon (18◦ 40  N, 88◦ 22 W and 18◦ 36 50 N, 88◦ 25 27 W) coll. 04.09.1997 by MEG and 27.09.1998 by NNS & MEG; Xul-ha lagoon near Bacalar (18◦ 34 N, 88◦ 26 W), nd, nd; Cenote Normal near Bacalar (18◦ 39 59 N, 88◦ 23 10 W), coll. 20.08.1997 by MEG; Cenote Azul near Bacalar (18◦ 38 48 N,

65

Figures 13–22. Macrothrix elegans, lectotype from Itatiba (13–15) and paralectotype from São Paulo (16), Brazil; details of parthenogenetic female from a small almost dried puddle near Carillo Puerto, Quintana Roo, Mexico, coll. 04.07.2002 by M. El´ıas-Guti´errez, A. A. Kotov & J. G. Granados-Ram´ırez (17–19) and a small puddle near Zoological garden, Belize, coll. 06.09.1997 by M. M. El´ıas-Guti´errez (20, 21): Figs 13–15, lectotype, its postero-ventral margin and head; Fig. 16, adult male; Figs 17–19, dorsal head pore, second segment of antennal exopod and postabdomen of adult from Quintana Roo; Figs 20–22, dorsal head pore, second segment of antennal exopod and postabdomen of adult from Belize. Scale bar denotes 100 µm for 13–16, 19, 22; 10 µm for 17–18, 20–21.

88◦ 14 42 W), coll. 25.06.1995 by MEG; three pools in a flooded savanna in the road to Majahual town (18◦ 57 44.8 N, 87◦ 55 01.2 W; 18◦ 49 12.1 N, 87◦ 46 54.9 W and 19◦ 28 07 N, 88o 01 46”W), 29.08.2001 coll. MEG, AAK & MAG; Noh bec lagoon (19◦ 05 53.9 N, 88◦ 12 19.2 W), coll. 30.04.1997 by MEG; El Padre lagoon in Sian Ka’an Natural Reserve (19◦ 36 23 N, 87◦ 59 17 W), coll. 03.03.2001 by MEG, AAK & ACM; a minicenote

near El Padre lagoon (19◦ 36 25 N, 87◦ 59 21 W), coll. 05.10.1998 by NNS & MEG and 03.03.2001 by MEG, AAK & ACM; an unnamed lagoon at km 157 of the highway Chetumal-Tulum (19◦ 45 38 N, 87◦ 54 15 W), coll. 16.03.2001 by MEG, AAK & ACM; a small, almost dried puddle near Felipe Carillo Puerto (19◦ 38 33 N, 87◦ 59 53 W), coll. 04.07.2002 by MEG, AAK & JGR. Yucatán State: Dzibalchatun sinkhole (21◦ 05 30 N, 89◦ 35 54 W),

66

Figures 23–31. Macrothrix elegans, parthenogenetic females from a small puddle, near Santa Fe city, Santa Fe, Argentina, coll. 05.07.1981 by N. N. Smirnov: Fig. 23, small adult; Figs 24–26, larger adult in lateral, antero-ventral and dorsal view; Figs 27, 28, dorsal head pore and reticulation of valve; Figs 29, 30, setae at postero-ventral portion of valves in outer and inner view; Fig. 31, postabdominal claws. Scale bar denotes 100 µm for 23–26; 10 µm for 27–31.

coll. 06.10.1998 by NNS & MEG; two localities in the shore zone of Chichancanab lagoon (19◦ 57 N, 88◦ 44◦ W & 19◦ 53 46.3 N, 88◦ 46 00.4 W), coll. 01.05.1997 by MEG and 30.08.2001 by MEG, AAK & MAG. Campeche State: temporary ponds in a flooded wetland near Sabancuy (18◦ 56 00 N, 91◦ 06 25 W & 18◦ 53 30 N, 91◦ 02 35 W), coll. 14.01.1998 by MEG & ICO; Silvituc lagoon (18◦ 38 05.7 N, 90◦ 17 08.9 W), coll. 14.01.1998 by MEG & ICO; a temporary puddle

near a school in Matamoros village, near Escárcega (18◦ 35 50 N, 90◦ 38 24 W), coll. 13.10.1998 by NNS & MEG; a series of puddles near Palizada village (18◦ 07 01.7 N, 91◦ 07 03.3 W; 18◦ 04 45.4 N, 92◦ 01 32.0 W & 18◦ 03 06.0 N, 91◦ 55 01.5 W), coll. 11.01.1998 by MEG & ICO. Tabasco State: Leona Vicario pond (17◦ 42 54 N, 91◦ 32 53 W), coll. 31.01.1999 by MGA & ACM; temporary ponds at km 3 and 3.5 of the road to Balancan (17◦ 55 N, 91◦ 42 W), coll. 30.01.1999

67

Figures 32–40. Macrothrix elegans, parthenogenetic females from a minicenote near El Padre lagoon, Sian Ka’an Natural Reserve, Quintana Roo, Mexico, collected 03.03.2001 by M. El´ıas-Guti´errez, A. A. Kotov & A. Cervantes-Mart´ınez: Figs 32–35, adult in lateral, anterior, ventral and dorsal view; Figs 36, 37, posterior portion of head, dorsal view, and dorsal head pore; Fig. 38, frontal head pore; Fig. 39, postero-dorsal portion of valves; Fig. 40, postabdomen in dorsal view. Scale bar denotes 100 µm for 32–35, 40; 10 µm for 36–39.

by MGA & ACM; a temporary puddle at km 138.7 of the highway Escárcega-Villahermosa (17◦ 47 N, 91◦ 50 W), coll. 13.10.1998 by NNS & MEG; a small temporary puddle near the Usumacinta river, at Escárcega-Villahermosa highway (17◦ 50 44 N, 91◦ 47 25 W), coll. 13.10.1998 by NNS & MEG; a pool in a flooded savanna at km 140 of the federal highway 186 (17◦ 54 50 N, 91◦ 45 50 W), coll. 01.02.1999 by MGA & ACM; El Espino lagoon (18◦ 13 26.3 N, 92◦ 19 18.6 W), coll. 13.01.1998

by MEG & ICO; a temporary pond at km 51 of the Villahermosa-Frontera highway (18◦ 23 52.3 N, 92◦ 47 0 W), coll. 30.01.1998 by MGA & ACM; El Guao Lagoon and a channel near it (18◦ 16 48.3 N, 92◦ 18 21.0 W & 18◦ 17 22,7 N, 92◦ 19 33 W), coll.13.01.1998 by MEG & ICO. Veracruz State: Temporary at km 90,2 of the Acayucan-Tinaja highway (18◦ 17 30 N, 95◦ 46 43 W), coll. 21.10.1998 by NNS & MEG.

68

Figures 41–52. Macrothrix elegans, parthenogenetic females from a puddle in Santa Fe, Argentina (41–46) and a pool near Rio Tipitapa, Nicaragua, coll. 17.05.1988 by N. N. Smirnov (47–52): Fig. 41, antenna I in latero-distal view; Figs 42–44, antenna II, its distal segment and swimming setae; Fig. 45, inner-distal portion of limb III; Fig. 46, inner portion of limb IV; Fig. 47, labrum in ventral view; Fig. 48, postero-dorsal portion of head; Fig. 49, left mandible; Figs 50, 51, antenna II and its largest lateral swimming seta; Fig. 52, distal portion of limb I. Scale bar denotes 100 µm for 41–42, 10 µm for 43–52.

All samples from Guatemala, Belize and Mexico are kept at ECO-CH-ZOO. Amended diagnosis Parthenogenetic female: In dorsal view, body regularly ovoid, dorsal margin finely serrated, with a shallow depression posterior to dorsal head pore. Posterodorsal angle in level of longitudinal body axis, from a pointed angle to a rounded triangle, but never like

a protruding short spine. Whole surface of head and valves covered with striae, with rare or numerous anastomousings. Body significantly compressed laterally, with sharp dorsal keel. Compound eye large, located within a low occular dome. Ocellus small (eye/ocellus = 3–3.5), located slightly closer to tip of rostrum than to eye. Dorsal head pore ovoid, small, with a thick ring around it. Labrum wide, with series of small tubercles at apex.

69

Figures 53–74. Macrothrix elegans, parthenogenetic females from Itatiba, São Paulo (type locality) (54–59, 63, 65–68, 70–71, 74) and Baia do Castelo, N of Corumb´a, Mato Grosso do Sul, coll. 23.04.1998 by G.-O. Brandorff (53, 60–62, 64, 69, 72–73), Brazil: Figs 53–55, postabdomen in lateral and dorsal view; Figures 56, 57, basal and distal portion of postabdomen; Figs 58, 60, postabdominal claw in outer view; Figs 59, 61, the same in inner view; Fig. 62, distal part of postabdominal seta; Figs 63–67, antenna I and its distal portion; Fig. 68, antenna II; Figs 69–71, its exopod; Figs 72, 73, largest lateral endopod seta in outer and inner view; Fig. 74, its fragment. Scale bar denotes 100 µm.

Postabdomen subovoid, with rounded distal extremity, distinct heel basally, and with sculpture as longitudinal lines on sides of postabdomen. Preanal margin with short transversal series of short to medium-sized setules, in basal portion these setules always longer and more robust. Postabdominal seta with short distal segment, no setules on basal segment. Postabdominal claw small, outer dorsal row of denticles consists only of ‘basal spine’ and second denticle located distally, medial ventral row of about 2–3 denticles, and inner dorsal row with numerous

denticles, two of them remarkably more robust than the rest. Antenna I rod-like, straight to slightly curved, sensory seta externally at a distance more than antennular diameter from antennule joint, about 7–9 short transverse rows of denticles on anterior surface of antennule. Nine short aesthetascs, two of them significantly larger than the rest. Antenna II with two small basal sensory setae of subequal size. Basal segment with bisegmented distal sensory seta reaching third exopod segment. Distal burrowing spine somewhat longer than basal segment of exopod, naked.

70

Figures 75–84. Macrothrix elegans, parthenogenetic females from a minicenote near El Padre lagoon, Mexico (75–82), and ephippial female from a small, almost dried, puddle near Carillo Puerto, Mexico (83–84): Figs 75, 76, antenna I and its esthetascs; Fig. 77, basal segment of antenna II; Figs 78–80, antenna II, its exopod and swimming setae; Fig. 81, distal portion of limb I; Fig. 82, scrapers on limb II; Figs 83, 84, ephippial female and its valve. Scale bar denotes 100 µm for 83–84; 10 µm for 75–82.

Swimming setae 0-0-1-3/1-1-3, spines 0-1-0-1/0-0-1. Length of apical swimming setae subequal, lateral setae on third segment of exopod and second segment of endopod longer than apical setae. Largest seta (on basal endopod segment) with series of robust, sparse spinules in middle portion, and a fringe of short setules in basal and distal portions. True spine on second segment of exopod with half length of this segment, or smaller. Additional spines on exopod segments vary

in size, but always form a series of elements, with size decreasing gradually in dorsal direction. On limb I, ODL with long apical seta, its distal segment unilaterally armed with sparse setules, and small, bilaterally setulated lateral seta; IDL with tree series of strong setules, and a group of fine setules more basally, and three bisegmented setae of different size, unilaterally setulated distally, two smaller hook-shaped; two ejector hooks of similar size; a remainder of gnathobase I with two fully setulated

71 setae. On limb II, exopodite a subovoid lobe with bilaterally setulated seta and two bunches of setules; eight scrapers with length increasing distally, scrapers 1-2 with more delicate feathering, 3–8 with robust denticles; a solitary seta near gnathobase absent. Filter plate II with four setae and a rudiment of fifth seta. On limb III epipodite with three long setae distally, seta 1 (shorter) and 2 (longer) with unilaterally setulated distal segments, seta 3 bilaterally setulated from base to tip, and only a single lateral seta 4. On distal endite, a hard seta located posteriorly, with fine setules basally and robust denticles distally, seta b clearly bisegmented, with distal part unilaterally armed with long, fine setules, seta c small, bisegmented, bilaterally feathered distally. Basal endite posteriorly with 3 bisegmented soft setae (d–f). No filter plate III. On limb IV pre-epipodite, epipodite and exopodite small, the latter with two distal setae of variable size among populations. A single small seta remainder of filter plate IV. On limb V pre-epipodite three-lobed, epipodite large, from globular to gigantic. Only a projection with single seta remainder of exopodite. Inner-distal portion with 3 setae, gnathobase not expressed. Ephippial female: Dorsal margin of valves never elevating over head, body compressed laterally, with thick dorsal keel. Most of valves modified into ephippium, supplied with a special ornamentation in the form of hexagonal-rounded cells, central part of each cell slightly inflated. Ephippium transparent and weakly chitinized, with slight brown pigmentation, with onetwo eggs. Adult male: Body elongated, dorsum regularly and very slightly curved, postero-dorsal angle sharp, almost right, lying upper to level of longitudinal body axis. Abdomen with small projections on dorsal margin. Postabdomen with postanal portion modified into large, tube-like projection with distal gonopores and subdistal postabdominal claws, protruding dorsodistally to rest of postabdomen. No reticulation on postabdomen. Postabdominal claw greatly reduced in size, like small triangular projection with serrated distal margin. Antenna I large, S-shaped, with short sensory seta, additional male seta only somewhat larger than sensory seta, and then series of 3-5 robust setules. At distal end, a special projection; nine esthetascs, two of them twice longer than the rest, located separately from the rest. Inner distal lobe I with three setae of female type, copulatory hook slightly and regularly bent, with three ridges on its tip.

Size: Juvenile and adult parthenogenetic females 280– 1100 µm, ephippial females 550–715 µm, adult males 300–410 µm. Redescription Adult parthenogenetic female Body of large female regularly ovoid in lateral view, with maximum height in the middle, height/length = 0.54–0.69, but this rate varies significantly in different populations. Dorsal margin as a regular arch from tip of rostrum to posteriormost point, only slightly breached by a low dome over compound eye, and a shallow depression posterior to dorsal head pore (this is not a border between head and rest of body). Dorsal margin of valves in the majority of females elevated slightly under dorsal margin of head (Figs 3, 24), or in some individuals not elevated at all, but in few populations (including type locality) this elevation quite significant (Figs 1, 13, 32). Postero-dorsal angle lies in level of longitudinal body axis, because dorsal and ventral margins are arched equally, its shape varies from a pointed angle (specially in younger adult females, see Fig. 23) to a rounded triangle (specially in larger adults, Figs 13, 24), but never like a protruding short spine. Whole surface of head and valves striated (Figs 1, 3, 6, 9, 23–26, 32–36), in lateral view, these striae located dorso-ventrally on valves, and approximately at angle of 45◦ on head. In the majority of populations these striae very distinct, almost without anastomouses. But in few populations, including type locality (Fig. 9), these lines are fine, with numerous anastomouses. There is a problem with interpretation of Sars’s material, because these samples are more than 100 years old, and, maybe finer lines are a result of their higher transparency after long time in alcohol. A small-scale serration present on dorsal margin of valves, and sometimes of head, some of these minute denticles are terminal points of carapace striae (Figs 9, 28, 39). Body significantly compressed laterally (Figs 2, 5), with sharp dorsal keel (Figs 2, 26, 33). No remarkable structures on valves or head. Head large, its length from tip of rostrum to border with valves/body length up to 0.6 times. In lateral view, dorsal margin generally evenly convex, with a low dome above eye (Figs 6, 15), ventral margin almost straight, with crossing ridges and a special robust projection at base of labrum. A special line

72

Figures 85–98. Macrothrix elegans, head appendages of parthenogenetic female from Itatiba (85–90), and limbs of female from Baia do Castelo (91–99), Brazil: Figs 85–89, different types of armature in the swimming setae of antenna II; Fig. 90, paragnaths, maxillae I and II; Fig. 91, limb I; Figs 92, 93, limb II and distal armature of its gnathobase; Figs 94–96, limb III, its distal endite and distal armature of gnathobase; Fig. 97, limb IV; Fig. 98, limb V. Scale bar denotes 100 µm.

(fold) from tip of rostrum to mandibular joint, under the compound eye, in region of antenna II. This line corresponds to a poorly expressed fornix (Fig. 2). Compound eye large, located within a low occular dome. Ocellus small, located slightly closer to tip of rostrum than to eye. In anterior view, rostrum slightly compressed laterally (Figs 2, 25, 33, 34), a small split-like frontal head pore close to frontal edge of rostrum (Fig. 38, arrow). In dorsal view, head narrowing anteriod. Posterior border of head shield as a widely rounded angle (Figs 5,

26, 35, 36). In dorsal view, surface of head shield with transversal striation. Dorsal head pore (‘dorsal organ’ or ‘window’ are more correct names, because no pore is really here, only a window of specialised cuticle) ovoid, small, with rough surface and a ring around it, located on posterior part of head shield (Figs 7, 17, 20, 27, 36–37, 48). Thickness of this ring varies among populations, but always thicker than reticulation lines. Labrum wide, spade-shaped in ventral view (Fig. 47). In lateral view (Figs 6–8), labrum approximately triangular, with series of small tubercles at apex,

73

Figures 99–123. Macrothrix elegans from Rio Arapiuns, tributary of Rio Tapaj´os, Par´a, coll. 04.12.1996 by G.-O. Brandorff (111, 114–123) and Itatiba (99, 101–106, 110), Brazil; Santa Fe (100, 107–108) and unknown locality of Sars (112–113), Argentina; a minicenote near El Padre lagoon, Mexico (109): Figs 99, 100, inner distal lobe of limb I; Figs 101–106, setae on endite 3 and forks on endites 2 and 1 of limb I of two individuals; Fig. 107, distal setae of exopodite III; Figs 108–110, epipodite of limb V; Figs 111, 112, ephippial female in lateral view; Fig. 113, in anterior view; Fig. 114, adult male; Figs 115, 116, its labrum and valve margin; Figs 117, 118, its postabdomen and gonopore; Fig. 119, 120, its antenna I and esthetascs; Fig. 121, 122, exopod and largest lateral swimming seta of antenna II; Fig. 123, distal portion of limb I. Scale bar denotes 100 µm.

and setulated distal labral plate (anterior plug, in terms of Dumont & Silva-Briano, 2000). Valve surface with a distinct vertical, rarely anastomousing striation. Dorsal margin finely serrated (Figs 9, 39). Ventral margin of valves arched, distinctly serrated. Marginal setae jointed to posterior sides of these denticles (Figs 10–12, 14, 29, 30). These setae variable in length and size in different individuals, but there is a general outline in the order of their sequence: there are two ventrally directed

setae between each laterally oriented one. The latter normally more robust, and jointed to first (anteriormost) denticle of the above-mentioned triplet. In few animals, this laterally oriented setae is partly absent. In anterior and posterior portion of ventral margin the order of seta alternation is not too accurate (Fig. 12). Thorax long, while abdomen short, supplied with transverse row of setules (Fig. 53). Intestine without convolutions.

74 Postabdomen subovoid in lateral view, low, evenly narrowed distally, with a rounded extremity, and a distinct heel (inflated base of postabdominal setae) basally. Ventral margin straight, with few rows of small setules, dorsal margin slightly bi-lobed. Postabdomen subovoid in ventral view, not compressed laterally (Figs 40, 55). The incision, which bilobes the postabdomen dorsal margin, located at level of proximal border of anus and separating anal and preanal margin (Figs 53, 55). The latter long, almost straight in distal and middle portion, and curved basally, with short transversal series of setules, relative size of which varies significantly among populations. In basal portion, these setules always longer and robuster. Anal margin with numerous rows of short setules, approximately of similar size and length, laterally to them there are series of finer setules (Fig. 57). Small postanal margin with a group of short setules. Clear sculpture as longitudinal lines on sides of postabdomen (Figs 19, 22, 40, 53–55) Postabdominal seta as long as postabdomen, massive, with short distal segment bearing rare long setules (Fig. 62). No setules on basal segment. Postabdominal claw small, directed distally, slightly and regularly bent dorsally, with roundedpointed tip and wide base in lateral view. On claw, outer dorsal row of denticles consists only of ‘basal spine’ and second denticle located distally, medial ventral row of about 2–3 denticles, and inner dorsal row with numerous denticles, two of them more robust than the rest (Figs 31, 57–59). Antenna I ‘rod-like’ in terminology of Smirnov (1992), straight to slightly curved (Figs 8, 41, 63– 67). Subapical external angulation (‘subapical ventral angulation’ in terms of Silva-Briano, 1998, but we consider this term not proper) well-expressed, sensory seta located here externally at a major distance than antennular diameter from antennule joint. With about 7–9 short transverse rows of denticles on anterior surface, distal denticles longer at tip, with nine short terminal aesthetascs, two of them significantly larger than the rest (Fig. 76), all with two minute ‘claws’ at the apex. At the end, series of minute spinules. Antenna II large, coxal region folded, concertinalike, with two small basal sensory setae of subequal size in middle part and rows of small setules on each fold (Figs 68, 78). Basal segment robust, bearing transverse rows of spinules, and long, bisegmented distal sensory seta at inner (posterior) margin (Fig. 79), this seta reaching third exopod segment.

Distal burrowing spine somewhat longer than basal segment of exopod, naked, located on outer (anterior) surface, close to the end of basal segment (Figs 50, 77, 78). Antennal branches long, only basal member of 4-segmented branch (exopod) shortened, all other segments elongated, with transverse rows of setules. Segments 2–3 of exopod subequal in size, while terminal segment longer than these two (Fig. 42). Endopod middle segment smaller than the rest. Swimming setae 0-0-1-3/1-1-3, spines 0-1-0-1/00-1. Length of apical swimming setae subequal, approximately equal to length of basal segment plus length of branch. Lateral setae on third segment of exopod and second segment of endopod somewhat longer than apical setae, while lateral seta on first endopod segment larger, protruding significantly behind all other apical or lateral setae. We find six different types of structures in the swimming setae. These are marked by letters from ‘a’ to ‘f’ on Figs 68, 72, 85– 89, see also Figs 44, 80. Setae of type ‘a’ armed with sparse setules in both proximal and distal segments (Fig. 85); those of type ‘b’ armed with a row spines at one side of proximal segment and a dense setulation in both sides of distal segment (Fig. 86); type ‘c’ has sparse setules and a single terminal spine at one side of proximal segment, and asymmetrically armed distally (Fig. 87). Type ‘d’ (Fig. 88) has small spinules and a larger spine in one side of proximal segment, while distal segment with sparse setules and a fringe of minute spines in the opposite side. Type ‘e’ has sparse spinules in the proximal segment, ending in a larger spine near the joint with distal segment, the latter with sparse setules. Within distal segment of each seta, with the exception of the largest one (‘type f’), there is a chitinous insertion near joint with basal segment. Largest seta (Figs 51, 72–74, 80) with series of robust, sparse spinules in middle portion, and a fringe of short setules in basal and distal portions (‘type f’ armature). These types of armature were consistent in all populations examined. Apical spines short, from slightly curved to straight (Figs 43, 50). Only a single true spine on all other branch segments, namely, a spine on second segment of exopod, this spine shorter than the half length of this segment. On all segments of exopod there are additional denticles, which sometimes are modified into spines, large in some populations. These ‘spines’ are homologous to the small denticles at segment ends (instead of true spines, which are jointed with segments). Because of these reasons, they were not

75 included into antennal formula, following Smirnov (1992). Earlier, the same conclusion was made for the chydorid Leydigia (Kotov, 2003): this genus presents also additional spines on antennal branches, which are modified denticles. So, we name these structures below as ‘additional spines’ in contrast to true spines. In the majority of populations additional spines on second exopod segment are small, significantly smaller than true spines (Figs 18, 68, 70, 71). In other populations additional spines are large, but they always form a series of elements, with size decreasing gradually into dorsal direction (as a result, first additional spine longer than second one, not more than 3 times), also, in this case, all spines regularly curved (Figs 21, 69, 79). Mandibles small, elongated, evenly dilated distally, with asymmetrical heads, protruding inwards. Molar surface of left mandible (Fig. 49), with posterodorsal zone covered by minute nipple-shaped projections, not organised in ridges; large projections along antero-ventral edge of molar surface. Right mandible was not studied under SEM, but no differences from M. tripecinata (see Kotov, 1999) were found under optical microscope. Paragnaths, as series of setulated projections near mouth (Fig. 90: pgn). Maxilla I as large projection bearing three long, fully setulated setae; a series of stiff setules on its posterior face seems to be a remainder of the fourth seta of maxilla I, found in other anomopods, i.e., M. tripectinata (Kotov, 1999). A setulated projection posteriorly to maxilla I is, most probably, maxilla II (Fig. 90: mxII), which was initially reported to be absent in the Anomopoda (Fryer, 1963), but then found in adult Acantholeberis and Ophryoxus (Fryer, 1974), and in embryos of many other anomopods (Kotov, 1996). Limb I large, epipodite supplying with long fingerlike projection (Fig. 91). ODL cyllindrical, a long apical seta with distal segment unilaterally armed with sparse setules, and a small, bilaterally setulated lateral seta. IDL massive, with tree series of strong setules, and a group of fine setules more basally, and three bisegmented setae of different size, unilaterally setulated in distal part, two smaller setae hook-shaped (Figs 47, 52, 81, 99–100). Endite III with seta ‘a’ long, curved, shortly setulated in distal part, setae b-c short, spine-like, bisegmented, setulated unilaterally in basal part, posteriorly a short bisegmented seta 1, with setulation varying among populations (Figs 101, 104). Endite II with three long bisegmented setae, setulated at their distal

parts, setae e-f with specially robust setules, and a fork 2 posteriorly, number of denticles on its more robust branch varies in animals within a population (Figs 102, 105). Endite I with two bisegmented setae (g–h) setulated with long, dense setules distally and short, sparse setules basally, and a posterior fork 3 (Figs 103, 106). Ejector hooks of similar size, bisegmented, with distal segments short, and bilaterally setulated. Two fully setulated setae at inner side of limb base, a remainder of gnathobase I, so-called maxillar process (see Kotov, 1999). Limb II: Epipodite globular to subovoid (Fig. 92). Exopodite, a subovoid lobe with two bunches of setules and a short, bilaterally setulated seta. At inner margin of limb, eight robust scrapers with length increasing distally, scrapers 1–2 with delicate feathering, 3–8 with robust denticles, sometimes setae 4, or 5, or both, bear a specially robust denticle subdistally (Figs 82, 92). Small sensillae near seta 1, 3 and between 4 and 5. Low hillocks, remainders of posterior row of elements, in distal limb portion, while a solitary seta near gnathobase absent (in contrast to M. tripectinata, see Kotov, 1999). Distal armature of gnathobase with four elements (Fig. 93). Filter plate with four setae with size decreasing gradually distally; basally to them, a small structure, probably, rudiment of fifth seta, also a specially small protuberance of unclear homology here. Limb III: Epipodite very small, globular (Fig. 94). Exopodite large and flat, with three long setae distally (Figs 94, 107), seta 1 (shortest) and 2 (longest) with unilaterally setulated distal segment, seta 3 bilaterally setulated from base to tip. We never saw specimens with seta 2 equal in size to other setae, like the one presented by Dumont et al. (2002: Fig. 74). Only a single lateral seta 4, bilaterally setulated from base to tip (in contrast to M. tripectinata, see Kotov, 1999), margin between lateral and distal setae undulated, with a fringe of setules. Distal endite (see discussion of its homology in Kotov, 1999) anteriorly with a series of setules, and three bisegmented setae 1–3, unilaterally feathered in distal part, small elements (receptors?) in distalmost position, and near seta 3 (Figs 45, 95). Posteriorly, three setae: seta ‘a’ hard, with fine setules basally and robust denticles distally, seta ‘b’ clearly bisegmented, with distal part unilaterally armed with long, fine setules, seta ‘c’ small, bisegmented, bilaterally feathered distally. Basal endite approximately equal in size to distal endite. Anteriorly, a large sensillum (as in other Mac-

76 rothrix, see Dumont & Silva-Briano, 1997), and 4 setae with size increasing basad (4–7), all bisegmented and bilaterally feathered distally. Seta 7 with distal segment longer than basal one. The remaining, with distal segment shorter than basal one. Posteriorly, 3 bisegmented soft setae (d–f), similar in size, with inflated basal portions and bilaterally feathered distal portions. Gnathobase unclearly demarcated from basal endite, with four elements: a bottle-shaped element (sensillum?) near its border, and two hooks plus a short bisegmanted seta distally (Fig. 96). Limb IV: Pre-epipodite small, globular, with a few robust setules, epipodite small and globular (Fig. 97). Exopodite small, with distal group of two bilaterally feathered setae (1–2), with size varying among populations: in the majority of populations these two setae are of similar size, but in others, one of them remarkably longer. At inner margin a row of four elements (1–4), seta 1 longest, setulated basally, and naked distally, each setae 2–4 with an inflated basal and elongated distal part, the latter pointed at the tip, bilaterally feathered. A small receptor is present near base of seta 1, 2 and 3, respectively (the latter is not visible in Fig. 97). Posteriorly, a row of five erect soft setae, similar in size (a–e), bilaterally setulated distally (Fig. 46). Distal armature of gnathobase, with 4 elements: a bottle-shaped to subovoid sensillum near border with basal endite; a large setae with inflated basal segment and elongated, fully setulated, distal segment; a heavy hook; and a small, naked, bisegmented and curved hook. Posteriorly, on gnathobase, a single small seta continues the posterior row of setae of the inner limb face, the sole remainder of a filter plate IV. Limb V: Three-lobed pre-epipodite with fine setules, epipodite large, from globular to very elongated, gigantic (Figs 98, 108–110). Only a projection with single seta remainder of exopodite. Inner-distal portion as large flap, fringed by setules, on inner margin three setae with size significantly increasing distally (1–3), gnathobase not expressed. Differences of juvenile female In contrast with adult, body without border between head and valves, with valve dorsal margin not elevating under head, and with very distinct, almost right postero-ventral angle (Fig. 4). Head larger than in female. Antennae I and II, swimming antennal setae, postabdominal setae, and marginal setae of valves

longer. Rows of setules on antennules and antenna weakly developed. Ephippial female In lateral view, body proportions as in parthenogenetic female of similar size, although dorsal margin of valves never elevating over head. In anterior view, body more compressed laterally, with thicker dorsal keel. Practically all valves modified into ephippium (Figs 83, 84, 111, 112), supplied with a special ornamentation in the form of hexagonal-rounded cells, central part of each cell slightly inflated. Relative size of cells varies between populations. In dorsal part, reticulation on type of parthenogenetic female retained, ventral border of valves not modified, but a demarcated line between modified and non-modified zones absent. Ephippium transparent, weakly chitinized, with brown pigmentation. A chitinized plate along dorsal margin. The majority of ephippia of M. elegans contains two eggs, sometimes only one egg. Adult male Body more elongated than in juvenile female of same size, with maximal height at the middle. Dorsum regularly, and slightly curved, postero-dorsal angle sharp, almost straight, ventral margin significantly more convex than dorsal one. Head smaller than that in juvenile female, with dorsal margin evenly arched, and ventral margin almost straight (Fig. 115). Dorsal head pore bigger than in female. Compound eye, ocellus, labrum as in female. Valves with well expressed reticulation on female’s type, ventral margin additionally chitinized (Fig. 116). Thorax as in female. Abdomen with small projections on dorsal margin (Fig. 117). Postabdomen different from female, because postanal portion modified into a large, tubelike projection with distal gonopores and subdistal postabdominal claws, protruding dorso-distally to rest of postabdomen (Fig. 117). Preanal margin significantly shorter than in female, with very small setules, clear bordered from anal margin, supplied with series of denticles. No reticulation on postabdomen. Postabdominal setae somewhat shorter than postabdomen, with a bunch of setules distally. Postabdominal claw greatly reduced in size, like small triangular projection with serrated distal margin (Fig. 118).

77 Antenna I large, S-shaped, not dilating distally, with a small subapical external angulation bearing a short sensory seta (Fig. 119). Immediately after this angulation, but on inner-anterior face, an additional male seta, small for a genus representative, only somewhat larger than sensory seta, and a series of 3–5 robust setules. Also, a series of setules in the middle of external margin present. At distal end, a special projection and nine esthetascs, two of them significantly large (twice longer than the rest), and located separately from the rest (Fig. 120). Antenna II as in female, but additional spines on exopod segments not too large, as in adult females (Fig. 121). Maxillules, maxillae, paragnaths, mandibles similar to female. Thoracic limb I: Only distal part modified, as compared with female (Fig. 123). Only a single seta was found on ODL, IDL with three setae of the female type, and a large, slightly and regularly bent hook, with three ridges on its tip (Fig. 123). Limbs II–V as in female. Size Brazil: Itatiba (type locality): lectotype 815 µm, juvenile and adult parthenogenetic females 385– 1020 µm (n = 100), minimal size of reproduction 490 µm. São Paulo: juvenile and adult parthenogenetic females 465–735 µm (n = 17), minimal size of reproduction 540 µm, adult male 380 µm (n = 1). Rio Arapiuns: juvenile and adult females 350– 750 µm (n = 25), ephippial female 660 µm (n = 1); male II 340 µm (n = 1), adult males 375–410 µm (n = 2). Argentina: unknown locality: juvenile and adult parthenogenetic females 280–1100 µm (n = 100), minimal size of reproduction 555 µm, ephippial females 555–715 µm (n = 40), adult males 300– 375 µm (n = 5). See also a maximum size of female in some other populations in Table 2. Short note on distribution and biology This is the most common Neotropical species of Macrothrix, which is present, probably, in all types of water bodies here. In many puddles and small ponds M. elegans is a dominant anomopod species. Macrothrix superaculeata (Smirnov, 1982) Smirnov in Brandorff et al., 1982: 97–100, Figs 88– 92 (Echinisca); Smirnov, 1992: 74, 77–80 (in partim), Figs 320–327, Pl. III: Figs 16–18, Pl. IV: Figs 19–24, Pl. 5: Fig. 30; Elmoor-Loureiro, 1998: 25.

Type locality: ‘flooded meadow near the village of Terra Santa’, lower Rio Nhamundá region, Pará, Brazil (locality 3 in Brandorff et al., 1982). Holotype: parthenogenetic female, MGU 2779. Paratype: female, ZIN 3049. Other material examined Brazil. Pará: 16 ♀♀ from a flooded meadow near the village of Terra-Santa, Rio Nhamundá region, coll. 04.07.1975 by G.-O. Brandorff, NNS-1997-162 (the rest of sample from which the type series was selected); 10 ♀♀ from another water body in the Nhamundá region, coll. 21.09.1975 by G.-O. Brandorff. Roraima: 37 ♀♀ from a flooded savana, Ilha de Maracá, coll. 22.06.1987 by E. N. Santos-Silva & B. Robertson, AAK2002-024; 14 ♀♀ from a grassy pool at Ilha de Maracá, coll. 24.09.1987 by E. N. Santos-Silva & B. Robertson, NNS-1997-094. Diagnosis Adult parthenogenetic female: Body of large adult females regularly ovoid in lateral view, with maximum height in the middle. Dorsal margin not as a regular arch, breached significantly by a high dome over compound eye (Fig. 126), and deep ‘step’ from dorsal head pore to posterior border of head shield (Figs 125, 141, 142). Dorsal margin of valves elevated significantly under dorsal margin of head. Postero-dorsal angle lies in level of longitudinal body axis, like a protruding short spine. Valves with very fine reticulation in form of hexagonal cells somewhat elongated dorso-ventrally (Figs 125, 127, 141), reticulation on head visible only in dorsum (Fig. 147) and in pre-labral zone (Figs 143, 145–146). Body significantly compressed laterally (Figs 143, 144), with well-expressed, sharp dorsal keel. Head large, with a valves/body length up to 0.7 times; ventral margin s-shaped, with clear reticulation, no projection at base of labrum, only small denticles. A fold from tip of rostrum to mandibular joint lies significantly upper to eye. Compound eye large, ocellus small, located closer to tip of rostrum than to eye. Dorsal head pore ovoid, large, with rough surface and a very thin ring around it, thinner than reticulation line (Figs 147–149). Labrum wide, subquadrangular, with minute tubercles at apex, reticulation at anterior margin, and small distal labral plate (Fig. 126).

78

Figures 124–140. Macrothrix superaculeata, parthenogenetic females from a flooded meadow near the village of Terra-Santa, Rio Nhamund´a region (type locality), coll. 04.07.1975 by G.-O. Brandorff: Fig. 124, juvenile; Figs 125, 126, adult and its head; Fig. 127, reticulation of valves; Figs 128–130, setae at antero-ventral, ventral and postero-ventral portions of valve; Fig. 131, postabdomen; Figs 132, 133, basal and distal portion of postabdominal seta; Figs 134, 135, postabdominal claws in outer and inner view; Figs 136–138, antenna I; Figs 139, 140, antenna II of adult and juvenile. Scale bar denotes 100 µm.

Valves with dorsal margin finely serrated (Figs 125, 150). Ventral margin of valves arched, distinctly serrated, marginal setae jointed to posterior sides of these denticles (Figs 128–130, 152). There is a general outline in the order of sequence of marginal setae: two ventrally directed setae, located between each laterally oriented one.

Postabdomen subovoid, elongated, with rounded extremity, and with distinct heel basally, dorsal margin bi-lobed (Fig. 131). Preanal margin long, slightly arched, with short transversal series of about 4 large setules (Figs 151, 154), specially robust in basal portion. Clear sculpture as longitudinal lines on sides of postabdomen (Figs 131, 151, 153).

79

Figures 141–149. Macrothrix superaculeata, parthenogenetic females from flooded meadow near the village of Terra-Santa, Par´a, Brazil (type locality) (141, 149), and flooded savana at Ilha de Marac´a, Roraima, Brazil, coll. 22.06.1987 by Santos-Silva & B. Robertson (142–148), Brazil: Figs 141, 142, adult in lateral view; Figs 143, 144, adult in ventral and dorsal view; Figs 145, 146, head in lateral and ventral view; Fig. 147, posterior portion of head dorsally; Figures 148–149, head pore. Scale bar denotes 100 µm for 141–146; 10 µm for 147–149.

Postabdominal seta as long as postabdomen, with very short distal segment, supplied with rare long setules (Figs 133, 155), and setulated long basal segment (Fig. 132). Postabdominal claw small, directed distally, slightly and regularly bent dorsally, outer dorsal row of denticles with different number of members, located in distal half of claw (Figs 134, 156), medial ventral row of about 2–3 distal denticles (Figs 134, 157), and inner dorsal row with numerous setules along all mar-

gin, two of them sometimes more robust than the rest (Figs 135, 157). Antenna I ‘rod-like’, slightly curved, subapical external angulation well-expressed (Figs 136, 145, 146, 158), sensory seta at a 1/5 of the total antennular length from the antenna I joint, 7–9 short transverse rows of denticles on anterior surface, distal denticles longer, at tip with nine short terminal aesthetascs, two of them significantly larger than the rest (Fig. 137), all

80

Figures 150–159. Macrothrix superaculeata, parthenogenetic females from Ilha de Marac´a, Brazil: Fig. 159, dorsal margin of valves; Fig. 151, ventral margins of valves and postabdomen; Fig. 152, ventral margin of valve in inner view; Figs 153, 154, postabdomen and its preanal margin; Fig. 155, distal portion of postabdominal seta; Figs 156, 157, postabdominal claws in lateral and latero-distal view; Fig. 158, antenna I; Fig. 159, antenna II. Scale bar denotes 100 µm for 153, 159; 10 µm for 150–152, 154–158.

with two minute ‘claws’ at the apex. At the end, series of minute spinules (Figs 137, 138). Antenna II significantly larger than that of M. elegans, coxal region with two basal sensory setae, unequal in size (Fig. 139). On basal segment, distal sensory seta protruding remarkably behind distal end of second exopod segment (Fig. 140), distal burrowing spine obviously longer than basal segment of exopod, naked (Figs 139, 159).

Antennal branches with elongated segments (Figs 160–162). Swimming setae 0-0-1-3/1-1-3, spines 0-10-1/0-0-1. Length of apical swimming setae subequal, approximately equal to length of branch. Lateral setae on third segment of exopod and second segment of endopod somewhat longer than apical setae, while lateral seta on first endopod segment very large. We found only 4 different types of structures in swimming setae, in contrast with M. elegans that has five. These are marked by letters from a to d in Figs 139, 174–176.

81

Figures 160–168. Macrothrix superaculeata, parthenogenetic females from Terra-Santa (type locality) (162) and Ilha de Marac´a (160, 161, 163–168), Brazil: Figs 160–162 antenna II; Figs 163, swimming setae; Figs 164, 165, inner distal lobe I; Fig. 166, limb III (EN = Endopodite; EX = Exopodite); Figs 167, 168, scrapers of limb II and inner portion of limb IV. Scale bar denotes 10 µm.

Setae of type ‘a’ with long setules on both segments, and a fringe of small spinules in the distal segment (Fig. 174). Type ‘b’ has a row of spines, ending in a largest one in the proximal segment, and only setules on distal segment. Type ‘c’ seems to be a combination of type ‘a’ and ‘b’, with spines in the proximal segment, and a fringe of spinules on distal segment, with setules only in the opposite side. Within distal segment of each seta, with the exception of the largest one, a chitinous insertion near joint with basal segment, similar to that in M. elegans. Largest seta (Figs 139, 163,

172, 173: d) with series of robust, sparse spinules in middle and distal portions, and fringe of short setules in basal portion (type ‘d’ armature). Apical spines short, a true spine only on second segment of exopod, this spine about 1/3 the length of its segment. On segments 1–3 of exopod there are large additional spines (Figs 139, 140, 159–162, 170, 171). On each segment, only first additional spine is large, massive, straight, conically narrowing distally. Second and following (if present) additional spines very small, in the majority of specimens 3–6 times less

82

Figures 169–184. Macrothrix superaculeata, antennae II and thoracic limbs of parthenogenetic female from Terra-Santa, Brazil: Fig. 169, exopod of antenna II of juvenile; Figs 170, 171, the same of juvenile; Figs 174–176, swimming setae; Figs 172, 173, largest lateral swimming seta; Figs 177–179, limb I and its distal portion; Fig. 180, limb II; Figs 181, 182, limb III and distal armature of its gnathobase; Fig. 184, limb V. Scale bar denotes 100 µm.

than first additional spine, but in some animals second spine is more reduced, about 10 times smaller than the first spine (Fig. 185). Limb I, epipodite with long finger-like projection (Fig. 177). ODL cyllindrical, a long apical seta with distal segment unilaterally armed, with sparse setules, and a small, bilaterally setulated lateral seta. IDL massive, with tree series of strong setules, and three bisegmented setae of different size, unilaterally setulated in distal part, two smaller ones hook-shaped (Figs 164, 165, 178, 179). Armature of endites as in M. elegans, only setae ‘a’ and ‘1’ seem to be shorter in the former. Two ejector hooks of similar size, biseg-

mented, with distal segments shortly and bilaterally setulated. A remainder of gnathobase I is present, with two fully setulated setae. Limb II: Epipodite with short finger-like projection (Fig. 180). Exopodite, a subovoid lobe with long, bilaterally setulated seta. Scrapers (Fig. 167) as in M. elegans. Distal armature of gnathobase with four elements, filter plate with four setae with size slightly decreasing distally and a rudiment of fifth seta. Limb III: Epipodite very small, globular (Fig. 181). On exopodite, seta 1 setulated only distally, with robust setules. Seta 2 slightly longer than 1, with unilaterally and robust setules on distal segment, and bilater-

83

Figures 185. AD1/AD2 ratio vs TO/BL ratio in different populations of Macrothrix.
 M. elegans; M. superaculeata.

Figures 186. Cluster analysis of different populations analysed for M. superaculeata and M. elegans.

ally and finely setulated basal segment (Fig. 166). Seta 3 bilaterally setulated from base to tip; seta 4 long. Inner limb portion and gnathobase as in M. elegans (Figs 181, 182).

Limb IV: Pre-epipodite small, globular, with a few robust setules. Epipodite small and globular (Fig. 183). Exopodite small, with distal group of two bilaterally feathered setae of unequal size. In general, inner portion of this limb as in M. elegans (Fig. 168),

12

11

10

9

8

7

6

5

4

3

2

1

Locality

Itatiba, São Paulo, Brazil M. elegans Unknown locality near São Paulo, São Paulo, Brazil M. elegans Unknown locality, Argentina M. elegans Rio Santa Fe, Santa Fe, Argentina M. elegans Lagoon with Nymphaea, Alta Verapaz, Guatemala M. elegans Bacalar lagoon, Quintana Roo, Mexico M. elegans Small puddle near Felipe Carillo Puerto, Quintana Roo, Mexico M. elegans Minicenote near El Padre lagoon, Quintana Roo, Mexico M. elegans Leona Vicario lagoon, Tabasco, Mexico M. elegans Temporary pond at km 3 of the road to Balancan, Tabasco, Mexico M. superaculeata meadow near Terra-Santa, Par´a, Brazil M. superaculeata Ilha de Maraca, Roraima, Brazil

M. elegans

Number of Species population

BH/BL

PO/BL

PP/BL

PP/PO

TO/BL

MS/SS

AD1/SS

AD1/MS AD1/AD2

0.62–0.65 0.039–0.043 0.104–0.121 2.43–2.93 0.012–0.016 0.32–0.42 0.15–0.19 0.40–0.50 1.00–2.00

557–685

500–702

507–600

564–657

50–660

542–628

496–596

478–642

592–715

0.61–0.65 0.031–0.044 0.115–0.143 3.00–3.62 0.030–0.043 0.36–0.52 0.28–0.54 0.71–1.14 3.50–5.00

0.62–0.69 0.031–0.044 0.125–0.160 3.00–4.03 0.026–0.038 0.31–0.40 0.32–0.42 0.80–1.27 3.57–9.75

0.64–0.69 0.020–0.029 0.111–0.129 3.88–6.00 0.022–0.033 0.41–0.53 0.26–0.39 0.50–0.85 1.33–2.80

0.61–0.65 0.023–0.030 0.110–0.116 3.89–4.80 0.013–0.021 0.43–0.58 0.10–0.19 0.18–0.44 1.05–2.67

0.59–0.64 0.012–0.021 0.101–0.119 4.80–9.33 0.020–0.029 0.41–0.56 0.19–0.33 0.38–0.71 1.50–2.00

0.56–0.63 0.014–0.019 0.091–0.124 5.00–7.25 0.014–0.022 0.45–0.60 0.13–0.23 0.22–0.50 1.00–1.67

0.54–0.63 0.016–0.022 0.116–0.123 5.00–7.25 0.012–0.019 0.43–0.62 0.18–0.23 0.33–0.44 1.25–2.00

0.54–0.63 0.016–0.027 0.092–0.127 3.57–6.25 0.018–0.026 0.47–0.63 0.20–0.44 0.43–0.86 1.00–2.10

0.58–0.65 0.019–0.026 0.113–0.152 5.25–6.67 0.014–0.018 0.36–0.44 0.12–0.19 0.30–0.50 1.13–1.50

814–1100 0.59–0.63 0.031–0.037 0.102–0.128 2.78–4.00 0.008–0.013 0.32–0.50 0.13–0.27 0.31–0.67 0.67–1.75

650–735

815–1015 0.60–0.65 0.031–0.039 0.102–0.120 2.94–3.63 0.011–0.017 0.30–0.46 0.12–0.17 0.33–0.56 1.25–2.10

BL, µm

Table 2. Ranges of certain values for different populations of M. elegans and M. superaculeata.

84

85 only the sensillum located at the base of seta 3, instead of seta 2. Limb V: Pre-epipodite tree-lobed, with fine setules. Epipodite elongated, gigantic (Figs 153, 184). Only armature of seta 1 and 2 on inner limb portion different from that in M. elegans, both are quite robust in M. superaculeata. Additionally seta 2 with stronger setules at distal segment. Juvenile female: Body subovoid, elongated, without spine at postero-dorsal angle, and with valves not elevated under head. In juvenile antenna I, a very robust first additional denticle on exopod segments 1–3 (Fig. 169). Ephippial female, male: unknown. Size: juvenile and adult females from Ilha de Maracá 410–750 µm (n = 37), adult females from Terra-Santa 620–780 µm (n = 14), up to 770 µm according to Smirnov (1992). Distribution: M. superaculeata was surely found only in the Amazon Basin, subsequent records from other South American localities, i.e. from Santa Fe by Smirnov (1992), most probably were superaculeatalike morphotypes of M. elegans. M. superaculeata is a significantly more rare species than M. elegans, and normally co-exists with M. paulensis, M. spinosa and Streblocerus pygmaeus.

Discussion Contrary to Smirnov’s (1992) key, many populations of M. elegans are also supplied with large additional spines on second segment of exopod. Dumont et al. (2002) were right, when they said that there are superaculeata-like morphotypes in populations of quite typical M. elegans. But these authors did not see the real superaculeata, which is quite specific, and not common species, relatively ‘local’ (Amazon basin) in the Americas. It differs from M. elegans in a series of characters (Table 3). Separation of the two species is also confirmed by discriminant function, and cluster analysis (Table 4, Fig. 186). But previously the discriminative features of both species were formulated intuitively (Brandorff et al., 1982; Smirnov, 1992). This was a reason of posterior misidentifications of M. superaculeata by Smirnov (1992). We specially tested a series of different relative parameters, originated from the size of the first additional spine on second segment of exopod, to find a hiatus between the two species. The discriminant analyses demonstrated as best variants the size of the

first additional spine relative to the size of the main (true) spine on second exopod segment (AD1/MS) (see Table 4 and Fig. 185). Also, it was important the relative size of AD1 to the length of second segment of antennal exopod (AD1/SS). After this analyses, it resulted in a single discriminant function, so it was not possible to graph it. Instead of this, we put a graph of the two more important variables that explained this discriminant function (AD1/MS vs. AD1/SS) . The classification matrix gave 100% of cases of both species correctly classified. However results of this analysis should be considered preliminary, because we run it with 93 elements of different populations of M. elegans vs. only 10 of M. superaculeata. Unfortunately there is no more material of superaculeata available at this moment. The ‘arc of spines’ (in terms of Fryer, 1974) in M. superaculeata is hyper-oligomerised, as compared with elegans-type: only a single spine is large, while others are almost completely reduced. The function of these additional spines is ‘probably to facilitate scrambling through vegetation’ (Fryer, 1974), and, maybe, differences in the organisation of the second antenna in two species is connected with different movement across the substrate. However, we think that it will be better to remove this character from a future key for the genus, and to replace it by characters of dorsal head pore, or setulation of basal segment of postabdominal setae, which are more obvious. Also, relative size of preanal teeth on postabdomen is helpful for species discrimination, but the hiatus between the two species is not too clear. We were not surprised to find that head pores are valuable for discrimination of congeners in Macrothrix, like in Chydoridae (Frey, 1959). Unfortunately, in many previous descriptions, authors reported only the presence of dorsal head pore, sometimes pointed on its size. Now, is clear that this part must be studied in more detail for all species of Macrothrix. Dumont et al. (2002) applied widely in their revision many characters of thoracic limbs, including size of epipodites, length and armature of some setae on exopodite and inner portion of different limbs, but we find that these authors were not right in the use of such features. For example, the size of epipodite V is a variable character. In M. elegans there are populations with globular, long, gigantic, and with medium-sized epipodites, and its size is varying significantly even within some populations. There is a chance, that size of epipodites on limbs could depend on the oxygen concentration in a water body, but this hypothesis must

86 Table 3. Differences between Macrothrix elegans and M. superaculeata. Character

M. elegans

M. superaculeata

Postero-dorsal angle like sharp spine Head pore with very fine ring, thinner than reticulation line Reticulation on valves

− − Vertical striae, sometimes anastomousing −

+ + Hexagonal +

− −

+ +

+ − − −

− + + +

Postabdomen, preanal denticles very robust, organised in only about 4 longitudinal rows Postabdominal seta with proximal segment setulated Antenna II, on second segment of exopod additional lateral spine very thick and longer than second additional spine more than in 3 times Antenna II short, at most reaching the half of total length On exopodite III seta 2 short On exopodite III setae 1 & 2 with robust setules distally On exopodite IV two setae of markedly different size

Table 4. Canonical analysis of several ratios of M. superaculeata and M. elegans. All cases were correctly classified by the model. Number of variables in model: 9; Wilks Lambda 0.199; F (9,99) = 41.49; p < 0.000.

Variable BH/BL PP/BL PP/PO TOO/BL MS/SS AD1/SS AD2/SS AD1/MS AD1/AD Eigenvalue Cum. Prop

Standardized coefficients for canonical variables

Factor structure matrix. Correlations variablescanonical roots (pooled- withingroups correlations)

Root 1 −0.393 0.414 −0.417 0.423 1.013 1.680 −0.815 2.327 0.161 4.016 1.000

Root 1 0.027 0.163 −0.164 0.442 −0.061 −0.274 −0.145 0.427 0.615

be checked accurately. Relative size of two setae on exopodite IV is variable among populations, and also this character is subjective, because the proportion between lengths of two setae depends on position of limb exopodite and the pressure by the cover slip: a seta closest to the observer seems to be longer. We are sure that limbs of Macrothrix bear a lot of informative structures for the genus systematics, but we

consider that fine peculiarities of setulation of some setae should be analysed carefully to uncover their variability in different populations of each species. We revealed that M. elegans is a variable species, some morphometric parameters differ significantly and their ranges frequently have no overlaps in different populations (Table 2). The cluster analysis of similarity between averages of all calculated parameters revealed differences between M. superaculeata and M. elegans, but did not reveal a geographical reason in the variability of M. elegans (Fig. 186, see specially the position of two different populations from Argentina, 3 and 4). Also it should be noticed that cluster 1–3 groups Sars’s laboratory cultures, instead of natural populations. We never find females with more than 750 µm total length in natural populations, while in Sars’ cultures the size was up to 1100 µm. Some female characters could be due to instar variability, a study which was out of the purpose of this article. Although we did not see males of M. superaculeata, we are sure that this is a member of the rosea-triserialis group, and we agree with Dumont et al. (2002) that this group is monophyletic. Maybe, this is a real a reason to return to Echinisca Lievin, 1848, now in subgenus status, following Petkovski (1973), but we are not going to make haste with the systematics of Macrothrix, which is at a stage of serious re-working now (Silva-Briano, 1998; Kotov, 1999; Dumont et al., 2002). In contrast to diverse fauna of rosea-like Macrothrix in Mexican highlands (Ciros-Pérez & Elías-Gutiérrez, 1996; Dumont et al., 2002), in the majority of Neotropical water bodies,

87 only M. elegans is present until now. Among Amazonian M. superaculeata, there is only other Neotropical species, which can be now surely assigned to roseagroup, namely M. marthaeby by (Elías-Gutiérrez & Smirnov (2000) but it seems to be an endemic of the Usumacinta river basin (Tabaso State, Mexico). At least, it was found in very limited samples, all of them related to lower Usumacinta in the South Mexico (pers. obs.). In this species, there is only a single additional spine on second exopod segment also, others are completely reduced (Elías-Gutiérrez & Smirnov, 2000: Fig. 14). So, this species is convergently similar with M. superaculeata.

Acknowledgements We are grateful to Prof. N. N. Smirnov for valuable comments and chance to examine many samples with Macrothrix, two anonymous referees for valuable comments and to Prof. H. J. Dumont for radical editing of the text. Special thanks to Dr Å. Wilhelmsen (GOS) and Dr A. Cabrinovic (NHM) for the sending of museum materials, to Dr G.-O. Brandorff, Dr W. Hollwedel, Dr H. Segers and Dr K. Van Damme supplying us by a bulk of the material from Brazil. Special thanks to Mr V. Antropov and G. Nieto for technical assistance in the work with SEM, and H. Bahena-Basave for the artwork in photographs. We thank A. Cervantes-Martínez, A. E. García-Morales, J. G. Granados-Ramírez, I. Castellanos-Osorio, M. Gutiérrez-Aguirre and M. A. Gololobova for assistance in the collection of samples in Mexico, Belize and Guatemala. AAK is very grateful to the Consejo Nacional de Ciencia y Tecnología for supporting his stay in Mexico, through the Catedras Patrimoniales program, and to authorities of El Colegio de la Frontera Sur for the logistic help. Part of this study was also supported by CONACYT-SEMARNAT grant No. C001-0051.

References Brandorff, G. O., W. Koste & N. N. Smirnov, 1982. Structure of rotiferan and crustacean communuties of the lower Rio Nhamundá, Amazonas, Brazil. Stud. Neotr. Fauna Inviron. 17: 69–121. Brehm, V., 1937. Brasilianische Cladoceren gesammelt von Dr. O. Schubart. Int. Rev. ges. Hydrobiol. 35: 497–512. Brehm, V., 1938. Nachträgliche Notizen zur Süßwasserfauna von Uruguay. Zool. Anz. 123: 26–32. Brehm, V., 1939. La fauna microscópica del Lago Petén, Guatemala. Anls. Escuela Nac. Cienc. Biol. 1: 173–204.

Brehm, V. & R. Thomsen, 1936. Brasilianische Phyllopoden und Arguliden gesammelt von Herrn Dr. O. Schubart. Zool. Anz. 116: 211–218. Ciros-Pérez, J. & M. Elías-Gutiérrez, 1996. Nuevos registros de cladóceros (Crustacea: Anomopoda) en México. Rev. Biol. Trop. 44: 297–304. Daday, E. von., 1905. Untersuchungen über die Süsswasser Mikrofauna Paraguays. Zoologica 44: 1–374. Delachaux, T., 1919. Cladocères des Andes Pèruviennes. Bull. Soc. neuchâtel. Sci. nat. 43: 18–38. Dumont, H. J. & M. Silva-Briano, 1997. Sensory and glandular equipment of the trunk limbs of the Chydoridae and Macrothricidae (Crustacea: Anomopoda). Hydrobiologia 360: 33–46. Dumont, H. J. & M. Silva-Briano, 1998. A reclassification of the anomopod families Macrothricidae and Chydoridae, with the creation of a new suborder, the Radopoda (Crustacea: Branchiopoda). Hydrobiologia 384: 119–149. Dumont, H. J. & M. Silva-Briano, 2000. Karualona n. gen. (Anomopoda: Chydoridae), with a description of two new species, and a key to all known species. Hydrobiologia 435: 61–82. Dumont, H. J., M. S. Briano & K. K. S. Babu, 2002. A re-evaluation of the Macrothrix rosea-triserialis group, with the description of two new species (Crustacea Anomopoda: Macrothricidae). Hydrobiologia 467: 1–44. Elías-Gutiérrez, M. & N. N. Smirnov, 2000. Macrothrix marthae, a new species (Crustacea: Anomopoda: Macrothricidae), a highly specialized macrothricid from Mexico. Proc. Biol. Soc. Wash. 113: 652–660. Elmoor-Loureiro, L. M. A. 1998. Branchiopoda. Freshwater Cladocera. In Young, P. S. (ed.), Catalogue of Crustacea of Brazil. Museu Nacional, Rio de Janeiro: 15–41. Frey, D. G., 1959. The taxonomic and phylogenetic significance of the head pores of the Chydoridae (Cladocera). Int. Rev. Ges Hydrobiol. 44: 27–50. Frey, D. G. 1982. Cladocera. In Hurlbert, S. H. & A. VillalobosFigueroa (eds.), Aquatic Biota of Mexico, Central America and the West Indies. San Diego State University, San Diego, California: 177–186. Fryer, G., 1963. The functional morphology and the feeding mechanism of the chydorid cladoceran Eurycercus lamellatus (O.F. Mueller). Trans. Roy. Soc. Edinb. 65: 335–381. Fryer, G., 1974. Evolution and adaptive radiation in the Macrothricidae (Crustacea: Cladocera): a study of comparative functional morphology and ecology. Phil. Trans. R. Soc. London B269: 137–274. Harding, J. P., 1955. Percy Sladen Trust expedition. XIX. Crustacea: Cladocera. Trans. Linn. Soc. Lond. 1: 329 – 354. Infante, A., 1980. Los cladóceros del Lado de Valencia. Acta Ciet. Venezolana 31: 593–603. Kotov, A. A., 1996. Fate of the second maxilla during embryogenesis in some Anomopoda Crustacea (Branchiopoda). Zool. J. linn. Soc. 116: 393–405. Kotov, A. A., 1999. Redescription of Macrothrix tripectinata Weisig, 1934 (Anomopoda, Branchiopoda), with a discussion of some features rarely used in the systematics of the genus. Hydrobiologia 403: 63–80. Kotov, A. A., 2000. Analysis of Kozhowia Vasiljeva & Smirnov, 1969 (Chydoridae, Anomopoda, Branchiopoda), and a description of Parakozhowia n. gen. Hydrobiologia 437: 17–56. Kotov, A. A., 2003. Separation of Leydigia louisi Jenkin, 1934 from L. leydigi (Schoedler, 1863) (Chydoridae, Anomopoda, Cladocera). Hydrobiologia 490: 147–168.

88 Montú, M. & I. M. Gloeden, 1986. Atlas dos Cladocera and Copepoda (Crustacea) do estuário da Lagoa dos Patos (Rio Grande, Brasil). Neritica, Pontal do Sul 1 (2): 1–134. Orghidan, T. & S. Negrea, 1973. Cladocères des eaux souterraines et épigées de Cuba (II). Résultats des expéditions biospéologiques Cubano-Roumaines à Cuba. Bucuresti: 105–115. Paggi, J. C. 1995. Crustacea Cladocera. In Lopretto, E. C. & G. Tell (eds.), Ecosistemas de Aguas Continentales. Metodología para su Estudio. Ediciones Sur, La Plata: 909–951. Petkovski, T. K., 1973. Zur Cladoceren-Fauna Australiens. II. Sididae und Macrothricidae. Acta Mus. Macedon. Sci. Natur. 13: 161–192. Sars, G. O., 1901. Contributions to the knowledge of the fresh-water Entomostraca of South America, as shown by artificial hatching from dried material. 1. Cladocera. Arch. Math. Naturv. 23: 1– 102. Silva-Briano, M., 1998. A revision of Macrothricid-like anomopods. Ph.D. Thesis, Ghent University, Gent, 388 pp. Smirnov, N. N., 1969. Morpho-functional grounds of mode of life of Cladocera. III. Oligomerization in Cladocera. Hydrobiologia 34: 235–242.

Smirnov, N. N., 1971. Morpho-functional grounds of mode of life of Cladocera. V. Morphology and adaptive modification of trunk limbs of Anomopoda. Hydrobiologia 37: 317–345. Smirnov, N. N., 1976. Macrothricidae i Moinidae fauni mira. Fauna SSSR. Rakoobraznie 1 (3): 1–237 [Macrothricidae and Moinidae of the World. In Russian]. Smirnov, N. N., 1992. The Macrothricidae of the World. Guides to the Identification of the Microivertebrates of the Continental Waters of the World 1. SPB Academic Publishing, Amsterdam, 143 pp. Stingelin, T., 1913. Cladoceren aus den Gebirge von Kolumbien. Mém. Soc. Neuchâteloise Sci. Nat. 5: 600–638. Valdivia Villar, R. S., 1988. Lista de Cladoceros dulceacuícolas del Perú. Amazoniana 10: 283–297. Van de Velde, I., H. J. Dumont & P. Grootaert, 1978. Report on a collection of Cladocera from Mexico and Guatemala. Arch. Hydrobiol. 83: 391–404.