(Podocopida: Limnocytheridae) from Mexican Crater Lakes Revista De Biología Tropical, Vol

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Cohuo-Durán, Sergio; Pérez, Liseth; Karanovic, Ivana On Limnocytherina axalapasco, a new freshwater ostracod (Podocopida: Limnocytheridae) from Mexican crater lakes Revista de Biología Tropical, vol. 62, núm. 1, mayo, 2014, pp. 15-32 Universidad de Costa Rica San Pedro de Montes de Oca, Costa Rica

Available in: http://www.redalyc.org/articulo.oa?id=44931382003

How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative On Limnocytherina axalapasco, a new freshwater ostracod (Podocopida: Limnocytheridae) from Mexican crater lakes

Sergio Cohuo-Durán1*, Liseth Pérez2 & Ivana Karanovic3 1. El Colegio de la frontera sur, Av. Centenario Km 5.5, 77014, Chetumal, Quintana Roo, Mexico; [email protected] 2. Instituto de Geología, Universidad Nacional Autónoma de México, Ciudad Universitaria, 04510, Distrito Federal, México; [email protected] 3. Hanyang University, Department of Life Science, Colleague of Natural Sciences, 17 Haengdang-dong, Seongdong- gu, Seoul 133-791, Korea; Institute of Marine and Antarctic Studies, University of Tasmania, Private Bag 49, 7001, Hobart, Tasmania, Australia; [email protected] * Correspondence

Received 12-III-2013. Corrected 10-VIII-2013. Accepted 11-IX-2013.

Abstract: Limnocytherina is a genus conformed by 12 species; its distribution in the American continent is known to be exclusively on the North (neartics), but little is reported about its distribution from Mexico (transition zone) and Central America (Neotropics). Different sampling campaigns were undertaken in three crater lakes from the Axalapascos region in east-central Mexico, during 2008, 2009 and 2011. As a product of these campaings, the new species of Limnocytherina axalapasco was found, which displays some intraspecific variability among populations. In this study, we described the taxonomy, the habitat, the ecological preferences and the larval development of this new species. A total of 10 sediment samples (8 littoral, 2 deepest point) were collected from lakes Alchichica, La Preciosa and Quechulac. We found that L. axalapasco is closely related to two North American species: L. posterolimba and L. itasca as well as one Central American species L. royi comb. nov. With the inclusion of L. axalapasco and L. royi to the genus, the distribution of Limnocytherina is extended to Central America. The four most important distinguishing characters of this new species are: 1) valve surface and margins covered with small, spine-like projections; 2) most of the A1 setae with a highly developed setule at distal part, producing a bifurcate appearance; 3) the upper ramus on the hemipenis is elongated, and by far overpasses dorsal/distal margins, distal lobe is triangular and short, while the hook-like process is prominent, outward orientated, and overpassing the tip of the distal lobe; 4) the UR is moderately developed with seta f3 elongated and setae f1 and f2 short. Considering its ecological characteristics and larval development, L. axala- - - + 2+ pasco was preferably found in alkaline waters dominated by Cl or HCO3 and Na or Mg , temperatures rang- ing between 19.1 to 20.3°C, and dissolved oxygen concentrations from 5 to 6.5mg/L. This species was abundant in deeper (~64m) areas of the saline Alchichica lake, where surface water displayed conductivity values of up to 2 250µS/cm, and the sand with low percentage of silt resulted the preferred substrate. Along with the description of L. axalapasco, we provide additional information on the hemipenis of L. itasca, L. royi and L. sanctipatricii, and we discuss on the Limnocytherina-type of hemipenis. Rev. Biol. Trop. 62 (1): 15-32. Epub 2014 March 01.

Key words: Ostracoda, taxonomy, ecology, Limnocytherina axalapasco, hemipenis.

Ostracods from Mexico and North Cen- Carreño, Ortega-Ramírez, & Alvarado-Valdez, tral America are poorly known, and so far the 2002; Chávez-Lara, Priyadarsi, Caballero, Car- majority of studies focused on paleolimnology reño, & Lakshumanan, 2012), only few stud- (Bridgwater, Heaton, & O’Hara, 1999a; Bridg- ies are dealing with taxonomy and ecology water, Holmes, & O’Hara, 1999b; Palacios-Fest, (Furtos, 1936; Tressler, 1954). Despite this,

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 15 22 species has been described in the region so species of the genus). According to Martens far, with most of the species (18) known from & Savatenalinton (2011) Limnocytherina cur- the Yucatán peninsula (Southern Mexico) and rently comprises 12 species, 11 being restricted North Guatemala, several of such species seem to North America (Delorme, 1971), and only to be endemic (Furtos, 1936; Furtos, 1938; Limnocytherina sanctipatricii has been found Brehm, 1939; Pérez, Lorenschat, Brenner, in Europe as well (Delorme, 1971; Meisch, Scharf & Schwalb, 2010a; Pérez et al., 2010b; 2000). The objective of this work was to pro- Pérez et al., 2011; Pérez et al., 2012; Cohuo- vide an accurate morphological description of Durán, Elías-Gutiérrez & Karanovic, 2013). this new species, and also include information From the Family Limnocytheridae, only one on its distribution, habitat, ecological prefer- species has been described in the region, Lim- ences and larval development. nocythere bradbury Forester, 1985, but nine species have been reported here. Limnocythere MATERIALS AND METHODS bradbury, L. friabilis Benson, & McDonald, 1963, L. staplini Gutentag & Benson, 1962, The ostracods were collected from the L. sappaensis Staplin, 1963, Limnocytherina crater lakes Alchichica, Quechulac and La Pre- itasca (Cole, 1969) and L. sanctipatricii (Brady ciosa, located in Puebla state, Mexico (Tables & Robertson, 1869) are known from North- 1, 2). Sampling campaigns were carried out central Mexico (McKenzie & Swain, 1967; during the dry seasons of December 2008 and Swain 1967; Forester 1985; Bridgwater et al., March 2009, and during the rainy season of 1999a; Maddocks, Machain-Castillo & Gío- June 2011. Sampling took approximately one Argáez, 2009), while Cytheridella americana day per study site. The samples were taken (Furtos, 1936), C. ilosvayi Daday, 1905, and from the limnetic and littoral zones, using Limnocythere opesta Brehm, 1939 are known plankton net (50µm mesh size, 30cm in diam- from Southern Mexico and Northern Gua- eter). Surface sediments containing ostracods temala (Furtos, 1936; Furtos, 1938; Brehm, were also collected from Alchichica and Que- 1939; Pérez et al., 2010a). Recent surveys of chulac lake’s deepest point (63m and 31.5m) the crater lakes in central Mexico revealed using Ekman grab. Sampling protocol follows one new species from the genus Limnocythe- Pérez et al. (2010a,b, 2011, 2012). All together, rina Negadaev-Nikonov, 1967. This genus we collected 10 sediment samples (8 littoral, was originally described as a subgenus of 2 lake deepest point samples; ca. 100mL wet Limnocythere Brady, 1868, but Martens (1996, sediment each) that were preserved in 96% 2000) subsequently raised its systematic posi- ethanol, and stored in 100mL PE-bottles for tion to a separate genus. He mainly focused on ostracod analysis in the laboratory. some distinct characters of the hemipenis (only Environmental variables of lake waters clearly described in the type species, Limno- (temperature, pH, dissolved oxygen, conductiv- cytherina sanctipatricii but not in the other ity, total dissolved solids (TDS) were measured

TABLE 1 Location and limnological characteristics of studied crater lakes where Limnocytherina axalapasco sp. nov. was collected

Lake N W Altitude (masl) Depth (m)* Surface area (km2) Secchi (m) Alchichica 19°24’37’’ 97°23’43’’ 2 322 64 (64)1 1.811 3.6-8.03,4 Quechulac 19°22’24’’ 97°21’00’’ 2 345 31.5 (39.1)1 0.291 3.64 La Preciosa 19°22’10’’ 97°23’14’’ 2 340 16.5 (45.5)2 0.782 4.6-64

*Maximal sampled water depth (Ekman Grab) and in parenthesis the lake deepest water depth. 1From Alcocer et al. (1998); 2From Juárez (2005); 3From Kaźmierczak et al. (2011); 4 From Ramirez & Vázquez (1998). Note: variables without reference were determined in this study.

16 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 with a Hydrolab Hach Quanta QD03594. Sec- DIC

C chi disc transparency at each lake was deter- (‰) 0.04 0.05 1.49 13

d mined at the lake deepest point. Parallel water samples were collected for water chemistry 2- - - 2- + + (‰) analysis (CO3 , HCO3 , Cl , SO4 , Na , K , 2+ 2+

-9.81 Mg , Ca ) which was carried out in the labo- -27.76 -28.19 SMOW

d D ratory at the Universidad Nacional Autónoma de México (UNAM). Stable isotopes (d18O, 13 (‰) d C, dD) in lake waters were measured at the Department of Geological Sciences, Univer- 1.35 SMOW -1.56 -1.18 O

18 sity of Florida. The detailed methodology is d in Pérez et al. (2010b). All samples were kept

2+ under refrigeration until previous analysis in 61 211 462 Mg the laboratory.

2+ At least 300 ostracod valves (equivalent to 11 12 20 Ca 150 specimen carapaces) were extracted under

+ a stereomicroscope Leica EZ4. Ten specimens 8 18 K 242 with well-preserved soft parts were dissected,

+ and soft parts mounted on microscope slides 91 Na 200

2 645 in Faure’s medium following the procedure proposed by Stock & Von Vaupel Klein (1996). -

Cl Drawings were made using a drawing tube 390 102 3 900 attached to an Olympus BX51 bright-field

2- compound microscope. Non-dissected mate- 18 128 SO4 1 013 rial was preserved in plastic tubes with 70% TABLE 2 TABLE ethanol. Ostracod valve measurements (n=100) - 3 and light microscope photographs were taken 497 265 739 HCO with a Canon Powershot A640 digital camera 2-

3 attached to a Zeiss Axiostar-plus light micro- 66 188 971 CO scope. Length and height were determined using the software AxioVision Release 4.6.3. 9 1.3 0.5

TDS The mean values and standard errors are in (g/L) table 3. Scanning Electron Microscope (SEM) photographs were taken with a Jeol JSM- 5600LV LCM scanning microscope from the 756 2 250 12 950 (µS/cm) Central Microscopy Laboratory, Institute of Conductivity Physics, Universidad Nacional Autónoma de

1 México. The examined material was deposited 6.5 5.0 6.5 in El Colegio de la Frontera Sur, Reference (mg/L) D. oxygen Zooplankton Collection (ECO-CH-Z, Acces-

pH sion numbers are provided). Hard parts were 9.3 8.9 8.9 also deposited at the Museo María del Carmen

Principal environmental variables and chemical composition (all in mg/L) of surface waters from studied crater lakes determined in June, 2011 lakes determined of surface waters from studied crater in mg/L) (all composition and chemical variables environmental Principal Perrilliat from Instituto de Geología de la Uni- (°C) 19.1 20.3 19.8 Temp. versidad Nacional Autónoma de México (IGM, accession numbers are provided). Eleven Lim- nocytherina itasca specimens were collected Lake from the littoral zone of a Tundra pond, Canada From Alcocer et al. (1998). From La Preciosa Quechulac Alchichica 1 (58°37’33” N - 94°13’42” W), in August 2006.

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 17 The analysis of COI gene for species compari- being longer than females and often expanded son is not presented here, because it was not posteriorly to accommodate a large hemipenis. possible to amplify the gene with the avail- A1 with the last segment fairly elongated with able primers (Folmer, Black, Hoeh, Lutz, & flagellated claws, A2 terminating with three Vrijenhoek, 1994; Schön, 2001; Martens, Ros- strong claws. Mxp strong and 2-segmented. setti, Butlin, & Schön, 2005) and because the Thoracic legs increasing in size (T1

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100 µm

200 µm

C D F

100 µm

200 µm H G

100 µm

Fig. 1. Limnocytherina axalapasco sp. nov. A - I, Holotype female. A, Right valve external view; B, Left valve external view; C, Right valve internal view; D, Left valve internal view; E, Antennula (A1); F, Antenna (A2); G, Maxilla (Mx); H, Maxilla with first endite modified; I, Maxillular palp (Mxp).

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 19 lakes (Alchichica, Quechulac, La Preciosa) are with selvage peripheral and abundant setae. located and where the ostracod species were Posterior margin projected downward (Fig. 5I) collected in high abundance (<240valves/ml with few long setae. Four muscular imprints on in surface sediments). The name should to be shell (Fig. 1C, D; 5B, E). treated as a noun in apposition. Soft parts: A1 (Fig. 1E). 5-segmented. Differential diagnosis: In both sexes sur- First segment with no setae, but with fringe of face valves reticulated, covered with small short and delicate setules on anterior margin, spine-like projections. In females the valves ending with six long setules antero-distally. are slightly downward projected posteriorly. Second segment bearing one apical serrulate A1 with the majority of setae with a long setule seta not reaching distal end of penultimate distally. A2 with spinneret (exopodite) not segment; anterior margin with several long reaching distal end of last segment. T3 sexu- and unequal setules. Third segment with one ally dimorphic, in females 5-segmented and apical anterior serrulate seta (with last setule with dp–seta reduced; in males 4-segmented elongated) reaching half length of last segment (last segment and claw fused) and with dp–seta (Fig. 2G, H). Fourth segment with two ser- swollen and strong. Hemipenis with distal lobe rulate setae situated medially, each one with a triangular and short; upper ramus elongated by long setule distally (Fig. 2G, H). Same segment far overpassing lateral/distal lobe; hook-like distally with four distinct setae. The most ante- process exceeding tip of distal lobe. UR mod- rior one simple seta clearly exceeding distal erately developed with claw-like f3. Posterior end of terminal segment. Following three setae part of the body of females with the uropod with a long setule almost at the end, producing bearing two seta; genital lobe cone-shaped end- a bifurcate appearance (Fig. 2G, H). Fifth seg- ing with a rounded tip. ment hirsute anteriorly; distally carrying three setae, longer one fused with aesthetasc; other Female (Holotype) two setae subequally long and with a long Hard parts: Carapace subrectangular. setule distally. Length ratios of four distal seg- Valves ornamented with nodes, concentrated ments 1.5:0.6:1.1:1. medially, in some specimens the nodes are A2 (Fig. 1F). 4-segmented. First segment modified into poor or well developed alar pro- with strong setules antero-proximally and short longations (Fig. 5C, F). Surface reticulate and setules along posterior margin; exopodite not covered with few, short, simple hair-like setae, reaching distal end of last segment. Second as well as few small spine-like projections (Fig. segment with one antero-apical serrulate seta, 1A, B; 2J), which are also present along mar- not reaching distal end of penultimate segment; gins. Marginal pore canal unbranched. Valves postero-proximally with group of setules. Third slightly asymmetrical with LV overlapping RV, segment with two unequal and serrulate setae anteriorly. LV (Fig. 1B, D), length 0.62mm postero-medially, longer one, just reaching dis- and height 0.27mm. Dorsal margin straight tal end of terminal segment. Antero-medially and covered with short setae. Ventral margin with the Y–aesthetasc and two unequal ser- slightly concave medially and postero-distally rulate setae, longer one just exceeding distal slightly downward projected. Anterior margin end of third segment. Antero-distally on the rounded with short setae. Selvage peripheral. same segment, two setae, one of them, long and Posterior margin downward projected with few strong, reaching distal end of terminal segment; setae. RV (Fig. 1A, C), length 0.61mm and second one smooth, half as long as previous height 0.25mm. Dorsal margin almost straight, seta. Fourth segment with three claws, two of covered with few setae. Ventral margin slightly them equally long, 2.2 times longer than termi- concave medially. Anterior margin rounded nal segment; third claw 2.6 times longer than

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100 µm 100 µm D 100 µm E F e

Uropodal ramus dp 100 µm

Genial dp 100 µm lobe

T3 100 µm G H I J Main seta

Setulae

Fig. 2. Limnocytherina axalapasco sp. nov. A - F, Holotype female. A, Mandible (Md); B, Mandibular palp (Mdp); C, First thoracic leg (T1); D, Second thoracic leg (T2); E, Third thoracic leg (T3); F, Uropodal ramus (UR) and genital lobe; G, A1, detail of setae; H, detail of distally elongated setule; I, Quechulac female valve ornamentation; J, detail of spine-like projections on surface valve.

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 21 terminal segment. Length ratios of last three end of terminal segment. Fourth segment end- segment 3.2:1.15:1. ing with a claw, 2.5 times longer than segment. Md (Fig. 2A). Mandibular coxa armed Basally this claw is bearing one short seta. with ten teeth and two teeth-like setae, short Length ratios of last three segments 2.1:1.1:1. simple seta present proximally on coxa. T2. (Fig. 2D). 4-segmented. Protopodite Mdp (Fig. 2B). 4-segmented. First seg- with three serrulate setae posteriorly. Most ment bearing exopodite composed of seven proximal seta, short and strong. Medial seta long plumose rays. Same segment anteriorly strong, exceeding distal end of the segment; bearing short serrulate seta not reaching distal apical seta short not reaching distal end of fol- end of segment. Second segment with five ser- lowing segment. Seta dp relatively short, thick- rulate setae at distal end, most anterior one by ened at its base. Second segment with e–seta, far exceeding distal end of terminal segment. exceeding distal end of penultimate segment. Most posterior ones subequally long overpass- Fourth segment bearing one long claw, which ing distal end of terminal segment. Two medial basally carries a small seta. Length ratios of last setae equally long and not reaching distal end three segments 2.2:1.2:1. of penultimate segment. Third segment antero- T3. (Fig. 2E). 5-segmented. First segment medially with two groups of serrulate setae, posteriorly with three serrulate setae, thickened proximal one with three equally long setae, at the base and unequally long. Seta dp tiny and distal one with two subequal setae exceeding smooth. Second segment with long and serru- distal end of terminal segment. Postero-distally late e–seta, just reaching distal end of penulti- three apical setae present, two of them short, mate segment. Fifth segment bearing short seta just exceeding distal end of last segment; third medially and ending with one elongated claw, seta smooth, 4.8 times longer than terminal 8.3 times longer than terminal segment. Length segment. Fourth segment with four unequally ratios of four last segments 6.2:3:2.4:1. long claw-like setae. Posterior part of body (Uropod) consisting Mx endites (Fig. 1G). Third endite ending of two unequal setae. Genital lobe cone-shaped with six short and strong teeth-like setae; a ending in a round tip (Fig. 2F). swollen and long seta situated medially. Sec- ond and first endites ending with six and seven Male (Allotype) teeth-like setae respectively; on proximal side of first endite two subequally long and simple Hard parts: Carapace sexually dimorphic, setae present. subrectangular anteriorly and widened poste- Mxp (Fig. 1I). 2-segmented. First segment riorly; marginal pore canals straight. Valves with short and sparsely distributed setules; with few nodes, sometimes modified into poor antero-apically one short and strong serrulate developed alar projections (Fig. 5D). Surface seta present, which exceeds distal end of ter- reticulated and covered with setae, and few minal segment. Posteriorly, four pappose setae small, spine-like projections covering surface present, longer one 6.2 times as long as termi- and margins. Valves slightly asymmetrical, LV nal segment. The two subequally long setae are is overlapping RV anteriorly. LV (Fig. 3A, D), 3/4 as long as longer seta. Smaller seta slightly length 0.66mm, height 0.36mm. Dorsal margin exceeds half length of longest seta. Second almost straight and covered with short setae. segment with three claw-like setae, subequally Ventral margin anteriorly straight with a poorly long, 3.4 times longer than segment. developed flange near medial region, posteri- T1 (Fig. 2C). 4-segmented. Protopo- orly widened (maximum wide at 3/4 of valve). dite hirsute and posteriorly armed with four Anterior margin rounded with abundant short unequally long serrulate setae. Seta dp short setae. Selvage peripheral. Posterior margin and strong, situated more proximal on segment. broadly rounded covered by short setae. RV Second segment with e–seta not reaching distal (Fig. 3B, C), length 0.65mm, height 0.34mm.

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100 µm

200 µm

C D

100 µm e dp

200 µm Fused segment

Upper ramus Dorsal margin

Distal lobe

dp I H Copulatory process

Hook-like organ f1 e f3 f2 Uropodal ramus

100 µm 100 µm

Fig. 3. Limnocytherina axalapasco sp. nov. A - I, Allotype male. A, Left valve external view; B, Right valve external view; C, Right valve internal view; D, Left valve internal view; E, Antenna (A1); F, First thoracic leg (T1); G, Second thoracic leg (T2); H, Third thoracic leg (T3); I, Hemipenis.

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 23 Dorsal margin straight and covered with setae. convex medially (Fig. 5O-R). In last instars, Ventral margin straight anteriorly and slightly valves are subrectangular with reticulate sur- concave around middle; posteriorly widened. face, often ornamented with bumps and some- Anterior margin with peripheral selvage and times with poor-developed alar prolongations. covered with setae. Posterior margin broadly Measurements of 100 adult (A) and juveniles rounded and covered with short setae. Four (A-6 to A-1) valves contained in the >63µm muscular imprints on shell (Fig. 3 C, D). fraction of surface sediments collected from the littoral zone of lake Alchichica, are shown Soft parts: A1 and A2 (Fig. 3E), without in figure 4. Besides, table 3 shows the mean sexual dimorphism, but on A2 the setae of length and height, and the standard errors for third segment and the claws of terminal seg- the different larval stages. Some intraspecific ment seem to be slightly more elongated than variability was observed in adult specimens: In in female. Terminal claws length as follows: Alchichica lake, one organism shows the third two subequally long claws 2.6 times longer endite of Mxp inwardly displaced, almost with than terminal segment; third claw is 2.8 times a hook-like appearance (Fig. 1H), this is prob- longer than terminal segment. T1 (Fig. 3F) ably a deformation of the specimen, but due similar to female, but one of setae situated on the highly specialized taxa encountered in this protopodite being simple, instead of serrulate lake, we provided this characteristic for further as in females. Terminal claw strong and longer analysis. Surface valves of specimens from than in females, 2.7 times longer than terminal Quechulac lakeare covered by a large num- segment.T2 (Fig. 3G) similar to female but dp– ber of spine-like projections (Fig. 2I, J), such seta slightly shorter. Distal seta on protopodite projections on specimens from the other lakes and e–seta shorter than in female. T3 (Fig. 3H) are scarce and sparsely distributed. Specimens 4-segmented and sexually dimorphic, dp–seta from Quechulac were also bigger than the ones swollen, pappose and long; e–seta more elon- observed in the other two lakes. gated than in female and exceeding distal end of terminal segment. Terminal claw elongated, Adult measurements: 7.1 times longer than terminal segment and Female basally not carrying any seta. • Quechulac: Length 0.71±0.004mm and Hemipenis (Fig. 3I). Body not very mus- height0.35±0.004mm (n=10). cular, with distal lobe triangular with blunt • La Preciosa: Length 0.67±0.005mm and tip; not prominent and not articulated. Dorsal height0.37±0.003mm (n=9). margin convex. Ventral margin square-shaped. • Alchichica: Length 0.64±0.008mm and Hook-like process strong, well sclerotized and height0.27±0.004mm (n=6). elongated, overpassing tip of distal lobe. Upper ramus elongated (tentacle-like appearance), Male sinuated anteriorly and rectangular medially • Quechulac: Length 0.75±0.006mm, and distally, tip rounded. Caudal ramus mod- height0.49±0.003mm (n=8). erately developed with f3 claw-like, setae f2 • La Preciosa: Length 0.71±0.005mm, and f1 short and thin. Copulatory process well height0.40±0.004mm (n=7). sclerotized and distally rounded. • Alchichica: Length 0.68±0.006mm, height0.36±0.004mm (n=11). Juveniles and adult variability: On ear- lier instars (

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A 320 A-1 A-2

A-3 280 A A-1 A-4 240

Heigth (µm) A-5 200 A A A-1 A-6 A-1 A-2 160 A-3 A-4 A-5 A-6 120 200 300 400 500 600 700 800 Length (µm)

Fig. 4. Scatter plot of length vs. height of larval stages of Limnocytherina axalapasco sp. nov. determined from measurements of 100 adult and juvenile valves collected from Lake Alchichica, east-central Mexico.

TABLE 3 Mean length, height and standard errors for the different larval stages of Limnocytherina axalapasco sp. nov.

Larval stage Length (mm) Height (mm) n A-6 0.26±0.002 0.15±0.002 3 A-5 0.33±0.003 0.19±0.002 16 A-4 0.40±0.004 0.22±0.002 22 A-3 0.48±0.004 0.26±0.002 21 A-2 0.54±0.006 0.27±0.003 10 A-1 0.59±0.005 0.29±0.003 11 Females 0.64±0.008 0.31±0.004 6 Males 0.68±0.006 0.29±0.004 11 upper ramus of the hemipenis (Fig. 6), which overpassing the dorsal margin, while in L. exceeds lateral and/or distal lobe and they also axalapasco sp. nov.it exceeds by far the same have a well-developed hook-like process. Their margin. In addition, the hook-like process is UR is moderately elongated (Cole, 1949; Hart- in L. posterolimba inwardly orientated and not mann, 1959). reaching tip of the distal lobe, while in L. axala- Limnocytherina posterolimba (Fig. 6F) pasco sp. nov. this part is outwardly orientated differs from L. axalapasco sp. nov. (Fig. 6A, B) and overpassing the distal lobe. The valves of mainly in some details of hemipenis. Namely, L. posterolimba have a depression around the the upper ramus in the former species is just posterior region and a well-developed flange

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 25 A B C

20 µm

D E F

20 µm

G H I

10 µm

J K L

10 µm

N M O

50 µm

P Q R 100 µm

Fig. 5. SEM pictures of adults and instars of Limnocytherina axalapasco sp. nov. from Lake Alchichica, east-central Mexico. A. Left valve (LV), external view, adult ♂; B. adductor muscle scars of ♂ (A); C. LV with bumps, external view, adult ♀; D. Right valve (RV) with bumps, external view, adult ♂; E. adductor muscle scars of ♀ (F); F. RV with bumps, external view, adult ♀; G. RV covered with diatoms, external view, adult ♂; H. Coccones, Amphora and Achnanthidium, diatoms (ID Caballero pers. comm.) on valve; I. Carapace, right side view, adult ♀; J. Carapace, ventral view, adult ♂; K. Valve ornamentation (I), external view; L. Carapace, ventral view, juvenile A-1; M. RV, external view, juvenile A-2; N. Marginal pore canals on LV, external view, adult; O. RV, external view, juvenile A-3; P. LV, external view, juvenile A-3; Q. LV, external view, juvenile A-4; R. RV external view, juvenile A-4.

26 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 A C E G

B D F H

Fig. 6. Hemipenis comparison of Limnocytherina species. A, B, Limnocytherina axalapasco sp. nov.; C, D, Limnocytherina itasca; E, Limnocytherina royi, modified after Hartmann (1959); F, Limnocytherina posterolimba, modified after Delorme (1971); G, Limnocytherina sanctipatricii, Scharf (pers. comm., 2013); H, L. sanctipatricii modified after Danielopol et al. (1989). Figures not to scale. postero-ventrally. Both characteristics absent in the tip of this lobe. This species also has an L. axalapasco sp. nov. elongated UR, almost reaching the tip of the Limnocytherina itasca (Fig. 6C, D) and hook-like process. L. axalapasco sp. nov. (Fig. 6A, B) also differ in details of the hemipenis morphology. In L. Species habitat description: The loca- itasca the upper ramus has at its base a small tion and principal limnological characteristics projection, which is more developed than in L. and environmental variables of the three crater axalapasco sp. nov. The distal lobe in L. itasca lakes and species habitat are included in tables is square-shaped. The hook-like process seems 1 and 2. In general, the three lakes displayed in to be articulated and does not reach the tip of June similar temperatures of the surface water the distal lobe. In L. axalapasco sp. nov. the (19.1-20.3°C), pH (8.9-9.3) and dissolved oxy- distal lobe is triangular-shaped and the hook- gen concentrations (5.0-6.5mg/L). Lake Alchi- like process (which is not articulated) over- chica (characterized by a semi-arid climate passes the tip of the distal lobe. The f2 seta on and a low annual precipitation <400mm) is the UR is more elongated in L. itasca than in L. the deepest (~64m) and the largest (1.8km2) axalapasco sp. nov. among the three studied lakes. It is a saline Limnocytherina royi comb. nov. (Fig. 6E) lake, displaying a high conductivity (12950µS/ and L. axalapasco sp. nov. (Fig. 6A, B) mainly cm) and TDS (9g/L); the water is dominated by differ in the hemipenis morphology. In the case chloride, sulfate, carbonate and sodium, mag- of L. royi the body of the hemipenis is com- nesium and potassium. Calcium is also present, pressed with the distal lobe almost rounded but in smaller concentrations. Water transpar- and with the hook-like process not reaching ency ranges from 3.6 to 8.0m. Lake sediments

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 27 are dominated by sand; Ramírez & Vázquez the lake Alchichica (239valves/mL in surface (1988) reported a high percentage (80.5%) of it sediments) than in lakes Quechulac and La in the sediments of Alchichica. Gravel, carbon- Preciosa. This suggests that the environmental ate and organic matter are also present but in conditions of Alchichica, i.e. more saline, are lower percentage. Typical aquatic vegetation favorable for this species. More specimens includes Ruppia maritima L., diatoms, filamen- were found in the littoral zone (~0.5m) than in tous chlorophytes and cyanophytes. The last deeper water (Quechulac, 31.5m). This species two are particularly abundant and they partially is benthic and it shows a preference for sandy cover the lake bottom (Alcocer, Escobar, Lugo sediments (≤80.5%). We also found abundant & Peralta, 1998). Lakes Quechulac and La adult carapaces with well-preserved soft parts Preciosa are smaller water bodies (≤0.78km2) (15carapaces/mL) in surface sediments from and are considered freshwater lakes. Their con- Lake Alchichica during our sampling in June ductivities are lower than those in Alchichica 2011, suggesting that in this lake species (<2250µS/cm). Quechulac surface waters are reaches adulthood during the summer period. dominated by bicarbonate, chloride, carbonate, Limnocytherina axalapasco sp. nov. was col- sodium, magnesium and calcium (Table 2). lected together with cladocerans, chironomids, La Preciosa is dominated by the same anions, trichopterans, amphipods, platyhelminthes and however magnesium, sodium and potassium thecamoebians. Other ostracod species found are the dominant cations in surface waters with L. axalapasco sp. nov. include Candona (Table 2). Oxygen, deuterium and carbon iso- sp. and Darwinula stevensoni (Brady & Rob- tope values in surface waters of Alchichica ertson, 1870). are more positive than those from Quechulac and La Preciosa. Stable isotopic composition DISCUSSION of surface water is very similar in Quechulac and La Preciosa. The sediments of these lakes Danielopol et al. (1989) divided the are mainly composed of sands (75.6%, 64.9%), Subfamily Limnocytherinae into four tribes, less percentage of silts (22.5%, 26.5%) and Limnocytherini, Dinarocytherini, Cytheridel- low concentration of organic matter (3.5%, lini and Leucocytherini. Martens (1996, 2000) 5.6%). Aquatic vegetation present in both revised the classification of Limnocytherini lakes includes Potamogeton pectinatus L. and and suggested that there are in fact three Ranunculus cymbalaria Pursh (Ramírez & different lineages: Limnocythere-lineage, Vázquez, 1988). Paralimnocythere-lineage and Neolimnocy- there-lineage. The same author preliminary Species ecological preferences: Data assigned the following three genera to the indicates that this species inhabits in waters Limnocythere-lineage: Limnocythere, Galo- with a broad range of salinity and therefore limnocythere Schornikov, 1973 and Limno- conductivity (756-12 950µS/cm), as well as cytherina. Karanovic (2012) highlighted the 2- - 2- the concentrations of CO3 , HCO3 , SO4 , necessity for a revision of these three genera, Cl-, Na+, K+ and Mg2+. Calcium content of because important morphological characters surface waters where the species was collected are still unclear in several species (poorly ranged from 11 and 20mg/L. The species seems described hemipenis and species known only to prefer waters with higher concentration after females) causing problems in the system- - 2- + 2+ of Cl or HCO3 and Na or Mg . The pre- atics of these genera. However, Limnocythe- ferred temperature ranges seems to be between rina can be distinguished from Limnocythere 19.1 and 20.3°C, the pH is alkaline (8.9-9.3), and Galolimnocythere based on morphology and the dissolved oxygen concentration was of the hemipenis, in which the characters are between 5.0 and 6.5mg/L. Limnocytherina well described only in the type species, Lim- axalapasco sp. nov. was more abundant in nocytherina sanctipatricii, while poorly known

28 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 or only inferred in others. After this study, the species and also for a clear understanding it became clear that on Limnocytherina the of its phylogeny. hemipenis morphology is varied. One specific Based on the current diagnosis of Limno- Limnocytherina-type of hemipenis, is the one cytherina, here we propose a new combina- observed in L. axalapasco sp. nov., L. itasca tion for Limnocytherina royi (Hartmann, 1959) and L. royi comb. nov. It is characterized by previously described in Limnocythere. This an elongated upper ramus, which also carries species is closely related to L. itasca and L. a large tentacle-like structure; lower ramus axalapasco sp. nov. (as pointed out above). It distally composed of lobes, forming a long has an elongated upper ramus on the hemipenis and thin hook-like process distally outward with a large tentacle-like structure, lower ramus displaced; and UR moderately enlarged bearing transformed into a hook-like process, and the three setae. In comparison with the hemipenis UR is moderately developed with f3 seta of Limnocytherina sanctipatricii (type species strongly developed. With the description of L. of Limnocytherina), the UR is the only char- axalapasco sp. nov. and the inclusion of L. royi, acter clearly shared among them. According to the current distribution of the Limnocytherina Meisch (2000), the enlargement of the UR is is much wider than considered in the past, one of the most important distinct characters because this genus was previously known only of Limnocytherina, but it needs to be pointed from North America. Limnocytherina axala- out, that different levels of UR enlargements pasco sp. nov. is from the transition zone of the can also be found in species of closely related continent (Neartic and Neotropical) and also genus such as Limnocythere opesta and L. potentially endemic to this region (previous elongata Delachaux, 1928, in which the UR studies of nearby lakes, as well as other water is also moderately developed (unusual feature bodies outside this region have not reported it) in Limnocythere). Although the morphology while Limnocytherina royi is a tropical spe- of UR is very important in the determination cies known from the Great lake of Nicaragua of species in Limnocytherina, it has to be (Hartmann, 1959). It is expected that intensive taken with caution and should be accompanied sampling of the transition zone and Central by other indicators of phylogenetic relation- America will reveal a number of new Limnocy- ships. Therefore, L. opesta and L. elongata therina species, hopefully providing important could not be transferred into Limnocytherina information for understanding the evolution of because they have some other characteristics the Limnocytherinae (Martens, 2000). on the hemipenis related to Limnocythere such Based on the ecological information as lower ramus triangular-shaped, strong and obtained from the field, L. axalapasco sp. nov. short and upper ramus reduced (Delachaux, may be considered as a good tool in paleo envi- 1928; Brehem, 1939). Limnocythere neotropi- ronmental reconstructions, because this species ca Klie, 1934, could be considered another was collected in a narrow temperature(~19- example of intermediate characters (strongly 20°C), pH (8.9-9.3), and dissolved oxygen developed hook-like process, lower and upper (5.0-6.5mg/L) ranges. It also has great potential reduced and UR developed as a separate struc- as a bioindicator for chemical composition of ture), which deserves a revision. Furthermore, water because it prefers water dominated by - 2- + 2+ distinct levels of enlargement of UR could Cl or HCO3 and Na or Mg . Future studies also be observed in the other lineages of the should focus on collecting ostracod samples tribe such as Neolimnocythere where the UR at different seasons of the same year, together is large to very large (Delachaux, 1928) and with the measurement of the environmental Paralimnocythere in which the UR is relatively variables. Experiments in the laboratory are large (Martens, 2000). The entire Limnocy- as well needed to determine the species toler- therinae deserve a revision and reevaluation ance to different ecological variables. This will of characters for an accurate classification of refine our observations and improve the use

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 29 of this species as a paleo environmental indi- (Instituto de Geofísica, UNAM), Socorro Loza- cator. The analysis of the communities of L. no, Alexander Correa-Metrio, Esperanza Torres axalapasco sp. nov. from the three crater lakes (Instituto de Geología, UNAM), María Aurora showed that adult specimens from the saline Armienta (Instituto de Geofísica), Jason Curtis lake Alchichica are smaller than those from (University of Florida, Gainesville) and Ana the lake La Preciosa. The largest adults were Lucía Martínez (Benemérita Universidad de collected from the lake Quechulac, which also Puebla). We also thank the agencies that pro- have a large number of small spine-like struc- vided financial support: CONACYT (project tures covering the entire shell surface (such number 167621), National Science Foundation number not observed in other specimens). (NSF award number 0902864). We appreci- These variability could be preliminary attrib- ate the constructive comments and drawings uted to adaptive responses to specific ecologi- provided by Burkhard Scharf, which helped in cal condition in each ecosystems, i.e. different the improvement of this manuscript. We also water chemistry of the lakes and the presence of appreciate the help of the institution involved highly specialized fauna composed of endemic in this research: El Colegio de la Frontera Sur, predators such as Poblana alchichica de Buen, Chetumal Unit, Hanyang University and Uni- 1945, Caecidotea williamsi Escobar-Briones & versidad Nacional Autónoma de México. Alcocer, 2002, Krizousacorixa tolteca Jansson, 1979 (Alcocer & Hammer, 1998; Escobar- Briones & Alcocer, 2002). However, Montiel- RESUMEN Martínez, Cirios-Pérez, Ortega-Mayagoitia & Limnocytherina axalapasco, un nuevo ostrácodo Elías-Gutiérrez (2008) demonstrated that in the dulceacuícola (Podocopida: Limnocytheridae) de lagos saline lake Alchichica, a speciation process has de cráter mexicanos. Limnocytherina es un género con- been taking place in copepods; the anterior was formado por 12 especies; su distribución en el continente highlighted by small morphological variability Americano se conoce exclusivamente en el norte (zona neártica), pero se sabe poco de su distribución en México among populations, as well as, reproductive (zona de transición) y Centro América (zona neotropical). behavior and molecular data. It is possible that Luego de diferentes campañas de muestreo en tres lagos similar speciation process could be occurring cráter de la región de los Axalapascos en la zona centro- in L. axalapasco sp. nov., expressed in the vari- este de México, durante 2008, 2009 y 2011, se encontró a ability observed among populations, but this Limnocytherina axalapasco, una nueva especie, que mos- tró variabilidad intraespecífica entre poblaciones. Un total should be careful further analyzed. de 10 muestras de sedimentos (8 del litoral, 2 del punto más During our sampling in June 2011, one profundo) fueron recolectadas de los lagos Alchichica, La potential reproductive period was observed, Preciosa y Quechulac. L. axalapasco esta estrechamente only male and female adults were collected relacionada con dos especies norteamericanas: L. postero- in high abundance in this month. Sampling limba y L. itasca, así como con una especie centroameri- campaigns developed during the other months cana Limnocytherina royi comb. nov. Con la inclusión de L. axalapasco y L. royi al género, la distribución de Lim- (December, March), reveal higher counts of nocytherina se extiende hasta Centro América. Los cuatro A-6 to A-1 instars than adult specimens sug- caracteres distintivos más importantes de esta nueva espe- gesting, a second reproductive period and it cie son: 1) superficie y márgenes de valvas cubiertos por is possible that juvenile specimens live at the pequeñas proyecciones parecidas a espinas; 2) La mayoría sampling location. de las setas de A1 tienen una setula muy desarrollada en la zona distal, con apariencia de estar bifurcadas; 3) El ramo superior del hemipene es alargado y por mucho sobrepa- ACKNOWLEDGMENTS sa los márgenes dorsal/distal; el lóbulo distal es corto y triangular, mientras que el proceso prensil es prominente, We thank those people who participated in orientado externamente y sobrepasa la longitud del lóbulo distal; 4) el UR esta moderadamente desarrollado con la our field trips, laboratory analyses, and com- seta f3 alargada y las setas f1 y f2 cortas. Para esta especie ments: Manuel Elías (ECOSUR, Chetumal se describe también su hábitat, preferencias ecológicas y Unit), Margarita Caballero, Edyta Zawisza desarrollo larvario. L. axalapasco prefiere aguas alcalinas

30 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 62 (1): 15-32, March 2014 - - + 2+ dominadas por Cl o HCO3 y Na o Mg , temperaturas Delachaux, T. (1928). Faune invertébrée d’eau douce des entre 19.1 a 20.3°C y concentraciones de oxígeno disuelto hauts plateaux du Pérou. Extrait du Bulletin de la de 5 a 6.5 mg/L. Esta especie es más abundante en las Société Neucháteloise des Sciences Naturelles, Nouv zonas profundas (~64m) del lago salino Alchichica, donde Sér, 1, 45-77. la conductividad del agua es de hasta 2 250µS/cm. Arenas Delorme, L. (1971). Freshwater ostracodes of Canada. Part con bajos porcentajes de limo parecen ser el sustrato prefe- V: Families Limnocytheridae, Loxoconchidae. Cana- rido. Aunado a la descripción de L. axalapasco, proveemos dian Journal of Zoology, 49, 43-64. información adicional para los hemipenes de L. itasca, L. royi y L. sanctipatricii, y discutimos el tipo de hemipene Escobar-Briones, E., & Alcocer, J. (2002). Caecidotea en Limnocytherina. williamsi (Crustacea: Isopoda: Asellidae), a new species from a saline crater-lake in the eastern Mexican Palabras clave: Ostracoda, taxonomía, ecología, Limno- Plateau. Hydrobiologia, 477, 93-105. cytherina axalapasco, hemipene. Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for amplification of mito- chondrial cytochrome c oxidase subunit I from diver- REFERENCES se metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294-299. Alcocer, J., Escobar, E., Lugo, A., & Peralta, L. (1998). Forester, R. (1985). Limnocythere bradburyi n. sp.: A Littoral benthos of the saline crater lakes of the basin Modern Ostracode from Central Mexico and a Pos- of Oriental, Mexico. International Journal of Salt sible Quaternary Paleoclimatic Indicator. Journal of Lake Research, 7, 87-108. Paleontology, 59, 8-20. Alcocer, J., & Hammer, U. (1998). Saline lake ecosystems Furtos, N. (1936). On the Ostracoda from the cenotes of of Mexico. Aquatic Ecosystem Health and Manage- Yucatan and vicinity. Publ. Carnegie Institution of ment, 1, 291-315. Washington, 457, 89-115. Brehm, V. (1939). La fauna microscópica del Lago Petén, Furtos, N. (1938). A new species of Cypridopsis from Guatemala. Anales de la Escuela Nacional de Cien- Yucatán. Publ. Carnegie Institution of Washington, cias Biológicas, 1, 173-203. 491, 155-157. Bridgwater, N., Heaton, T., & O’Hara, S. (1999a). A Garm, A. (2004). Revising the definition of the crustacean late Holocene paleolimnological record from central seta and setal classification systems based on exa- Mexico, based on faunal and stable-isotope analysis minations of the mouthpart setae of seven species of of ostracod shells. Journal of Paleolimnology, 22, decapods. Zoological Journal of the Linnean Society, 383-397. 142, 233-252. Bridgwater, N., Holmes, J. A., & O’Hara, S. (1999b). Com- Hartmann, G. (1959). Beitrag zur Kenntnis des Nicara- plex controls on the trace-element chemistry of non- gua-Sees unter besonderer Berücksichtigung seiner marine ostracods: an example from Lake Pátzcuaro, Ostracoden (mit Beschreibung von 5 neuen Arten). central Mexico. Palaeogeography, Palaeoclimatolo- Zoologischer Anzeiger, 162, 269-294. gy, Palaeoecology, 148, 117-131. Juárez, D. (2005). Registro de cambios paleoambientales Chávez-Lara, C., Priyadarsi, R., Caballero, M., Carreño, A. en sedimentos del lago “La Preciosa”, Puebla, con L., & Lakshumanan, C. (2012). Lacustrine ostracodes base en el estudio de ostrácodos. (M.Sc. unpublished from the Chihuahuan Desert of Mexico and inferred Late Quaternary paleoecological conditions. Revista thesis). Universidad Nacional Autónoma de México, Mexicana de Ciencias Geológicas, 29, 422-431. México. Cohuo-Durán, S., Elías-Gutiérrez, M., & Karanovic, I. Karanovic, I. (2012). Recent freshwater Ostracods of (2013). On three new species of Cypretta Vávra, 1895 the World. Crustacea, Ostracoda, Podocopida. Ger- (Crustacea: Ostracoda) from the Yucatan Peninsula, many: Springer-Verlag Berlin and Heidelberg. Mexico. Zootaxa, 3636, 501-524. Kaźmierczak, J., Kempe, S., Kremer, B., López-García, P., Cole, G. (1949). A New Cytherid Ostracod from Min- Moreira, D., & Taver, R. (2011). Hydrochemistry and nesota. Transactions of the American Microscopical microbialites of the alkaline crater lake Alchichica, Society, 68, 350-354. Mexico. Facies, 57 (4), 543-570. Danielopol, D. L., Martens, K., & Casale, L. M. (1989). Klie, W. (1934). Zur Kenntnis der Ostracoden-Gattung Revision of the genus Leucocythere Kaufmann, 1892 Limnocythere. Arch Naturgesch, Z Wiss Zool, Abt B, (Crustacea, Ostracoda, Limnocytheridae), with the 3, 534-544. description of a new species and two new tribes. Maddocks, R., Machain-Castillo, M., & Gío-Argáez, F. Bulletin de L’Institute Royal des Sciences Naturelles (2009). Podocopan Ostracoda (Crustacea) of the Gulf de Belgique, 59, 63-94. of Mexico. In D. Felder & D. K. Camp (Eds.). Gulf of

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