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Zookeys 911: 21—49 (2020)

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New distribution records of subterranean crustaceans from cenotes in Yucatan (Mexico)

Dorottya Angyal'?, Efrain M. Chavez-Solis'?, Luis A. Liévano-Beltran',

Benjamin Magafa', Nuno Simoes'*, Maite Mascaré!°

| Unidad Multidisciplinaria de Docencia e Investigacién, Facultad de Ciencias, Universidad Nacional Auténo- ma de México, Puerto de abrigo S/N, C.P 97356, Sisal, Yucatan, Mexico 2. Department of Zoology, Hungarian Natural History Museum, Baross u. 13, 1088 Budapest, Hungary 3 Posgrado en Ciencias Biolégicas, Univer- sidad Nacional Auténoma de México, Avenida Universidad 3000, Copilco-Universidad, Ciudad de México 04510, México 4 Posgrado en Ciencias del Mar y Limnologta, Universidad Nacional Auténoma de México, Avenida Universidad 3000, Copilco-Universidad, Ciudad de México 04510, México 5 Laboratorio Nacional de Resiliencia Costera, Laboratorios Nacionales (LANRESC), CONACYT, Puerto de abrigo S/N, C.P 97356, Sisal, Yucatan, Mexico 6 International Chair for Ocean and Coastal Studies, Harte Research Institute, Texas A&M at Corpus Christi, Texas, USA

Corresponding author: Maite Mascaré (mmm@ciencias.unam.mx)

Academic editor: Saskia Brix | Received 28 October 2019 | Accepted 3 January 2020 | Published 12 February 2020 http://zoobank.ore/491 BA314-A203-4D45-BIDF-CDA9398CA0AO

Citation: Angyal D, Chavez-Solis EM, Liévano-Beltran LA, Magafa B, Simoes N, Mascaré6 M (2020) New distribution records of subterranean crustaceans from cenotes in Yucatan (Mexico). ZooKeys 911: 21-49. https://doi.

org/10.3897/zookeys.91 1.47694

Abstract

New records of 14 stygobiont crustacean species pertaining to six Malacostraca orders from 32 cenotes are presented, with their associated caves of the state of Yucatan, Mexico, together with an individual account for each species. Species composition of most of the investigated cenotes is examined for the first time. A thermosbaenacean and two amphipod species were not formally recorded to the cenote ecosystems of the state of Yucatan prior to our research. Distribution data of a cirolanid isopod previously known only from its type locality is also provided. Barcodes of mitochondrial cytochrome c oxidase subunit I for the reported peracarid species previously lacking this information have been included in present study as tools

for species identification and a baseline of further molecular genetic analyses.

Keywords anchialine ecosystems, barcode sequences, biodiversity, endemic, Eucarida, Peracarida, stygobiont, Yu-

catan Peninsula

Copyright Dorottya Angyal et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

22 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

Introduction

’Cenotes’ (the local name for water-filled sinkholes) are typical karst features of the Yucatan Peninsula in Mexico. In many cases, far-reaching networks of submerged sub- terranean cave passages extend from them (Mercado-Salas et al. 2013). Due to the mixing of fresh and saline water, a distinct stratification can be observed inside these anchialine systems (Bishop et al. 2015). Intrusion of saline water is found deeper as the distance from the coastline increases (Bauer-Gottwein et al. 2011). Therefore, most inland cenotes within the state of Yucatan are exclusively freshwater systems, except for a few rather deep ones with haloclines below 50 m in depth, and those located near the northern coastline of the Peninsula (Alvarez et al. 2005; Angyal et al. 2018).

Anchialine ecosystems in Yucatan contain a crustacean-dominated fauna that is adapted to hypogene conditions, such as the lack of sunlight and the low food resource availability (Mejia-Ortiz et al. 2013). Stygobiont species are restricted to aquatic sub- terranean habitats (Botosaneanu 1986), and often exhibit conspicuous morphological adaptations to hypogene life, known as troglomorphisms. Such adaptations include structural reductions (e.g., loss of visual organs and pigmentation) or extensions (e.g., lengthening of appendages and complexity of sense organs) (Mejia-Ortiz et al. 2006; Gonzalez et al. 2018) and physiological modifications (e.g., reduced metabolic rates and starvation resistance) (Hervant et al. 1999, 2001; Bishop and Iliffe 2009). In 2016, prior to our systematic sampling, 47 stygobiotic crustacean species had been reported from anchialine ecosystems of the Mexican federal states of the Yucatan Peninsula, of which 22 were known from cenotes and submerged caves of the state of Yucatan (e.g., Holsinger 1977; Kallmeyer and Carpenter 1996; Alvarez et al. 2005; Sudrez-Morales et al. 2006). Fourteen percent of these species belong to the subclass Copepoda (9 spp.), while the remainder belong to the orders Mysida (1 sp.), Stygiomysida (2 spp.), Amphipoda (1 sp.), Isopoda (5 spp.), and Decapoda (4 spp.).

According to the database of the Secretaria de Desarrollo Sustentable (SDS Yu- catan), there are more than 3,000 registered cenotes and caves within this state. Cur- rent efforts are being directed to complete the descriptions of all registered cenotes, despite that only a small fraction of them have been biologically investigated to date. Ongoing research and explorations are necessary to describe the true biodiversity of these subterranean habitats, their geographical patterns, and changes in time. Thus, our aim was to improve our knowledge on the distribution and ecology of the stygo- biotic crustacean fauna of the cenotes and their associated cave passages in the state of Yucatan. We aimed to provide data from cenotes that had never been investigated from a zoological point of view in order to extend the geographical range of crustacean species distribution and contribute to a precise biodiversity mapping of stygofauna in Yucatan. Additionally, we intended to collect samples for molecular and morphologi- cal studies so as to gain and make available to the public mitochondrial cytochrome c oxidase subunit I sequences (COI) of species that were lacking barcode information, setting the standard for studies and tools for species identification.

25

New distribution records of subterranean crustaceans from cenotes in Yucatan

Materials and methods

Sampling sites and sampling

We collected stygobiotic macro-crustaceans from 32 cenotes between May 2016 and January 2018 in cenotes of the state of Yucatan (shorter form: Yucatan) (Figure 1, Table 1). Most of the cenotes studied are several kilometers away from the coast and contain only freshwater. In contrast, some cenotes near the coast have a halocline that divides the cave into freshwater and saline water habitats. Some of the cenotes studied belong to the ’Ring of Cenotes’, a fracture zone with high density of sinkholes identi- fied as the outer rim of the crater where the famous asteroid impacted Chicxulub 66 million years ago (Gonzalez-Herrera et al. 2002; Bauer-Gottwein et al. 2011) (Figure 1). Macro-crustaceans were collected during scientific cave dives using 50 ml sample

Table |. Location data and identification codes of the studied cenotes.

Cenote nr. (see | Cenote name | CenoteAndo Municipality Settlement Coordinates Coordinates

Figure 1 map) cenote code latitude longitude

1 Ayun-Nah 01980007Y_ Cacalchen Cacalchen 20°58'49.6"N 89°14'39.4"W 2 Bebelchen 00028064YC Uman Sanahcat 20°44'11.4"N | 89°43'55.4"W 3 Cervera 00090028YC | Dzilam de Bravo Yalsihom 21°22'29.5"N 88°50'01.8"W 4 Chihuo Hol 00080001YC Abala Mucuyche 20°38'06.1"N_ | 89°36'42.3"W 5 Dzalbay 00585085YC Temozon Dzalbay 20°49'53.4"N_ | 88°03'23.0"W 6 Dzonbakal 00125101YC Uman San Antonio Mulix | 20°40'11.4"N_ | 89°46'43.9"W 7 Dzonotila 00168001YC Abala Mucuyche 20°37'44.0"N_ | 89°39'33.0"W 8 Flor de Liz - Tixkokob Tixkokob 21°00'16.0"N_ | 89°23'33.0"W 9 Ixim Ha 00164037YC Tixkakal Tixkakal 20°37'49.0"N_ | 89°06'40.0"W 10 Kakuel 00142001YC Abala Mucuyche 20°37'40.3"N | 89°34'26.8"W 11 Kampepen 00042076YC Tecoh Chinquila 20°42'00.8"N 89°22'41.6"W 12 Kankirixche 00002001YC Abala Mucuyche 20°38'13.8"N 89°37'58.8" W 13 Kankal - Homun Homun 89°16'42.5"W 14 Kanun 01730036Y_ Homun Homun 20°44'44.2"N 89°14'40.7"W 15 Nayah 00009076YC Tecoh Pixyah 89°24'16.9" W 16 NoWChunck 00229011YC Chunchumil Celestun 20°48'48.5"N | 90°11'47.8"W 17 Nohmozon 00010076YC Tecoh Pixyah 89°38°42.0°W 18 Pixton 20°43'13.3"N_ | 89°10'08.5"W 19 Pol Box 00321023YC Chochola Chochola 20°41'24.3"N | 89°48'54.5"W 20 Sabtun 1 20°51'00.7"N_ | 90°14'08.1"N 21 San Elias 01171036Y_ 20°41'21.0"N 89°14'19.0"W 22 San Juan 00063036YC 20°44'02.6"N 89°17'18.6"W 23 Santito 00108045YC 20°38'58.1"N 89°53'44.3"W 24 El Virgen - 20°32'01.9"N_ | 89°02'19.4"W 25 Tres Oches - 20°43'55.7"N_ | 89°16'20.0"W 26 Tza Itza 00050076YC 20°43'49.1"N | 89°27'57.9"W 27 Xaan 00423036YC 20°43'39.3"N | 89°15'24.6"W 28 X’baba 00162023YC Chochola Chochola 20°40'42.5"N_ | 89°49'00.7"W 29 X-Barun 20°40123.8°N_ | 89°4622.8°W 30 X’kokob 00650093YC Ekmul Ekmul 20°56'51.0"N 89°20'41.0"W 5 Val Ue 5362407W 32 Yax-Kis 00091001YC Abala Mucuyche 89°35'35.7"W

24 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

90°0'W 89°0O'W 88°O'"W z Zz oO Cenote surveyed =) N CN N Cenote records fan OE RAS Geohydrological Reserve Ring of Cenotes z = = ey Al ~~ 23) YUCATAN = = ne ag & |. CAMPECHE g

QUINTANA ROO

90°0'W 89°0'W 88°0'W

Figure |. Map of the state of Yucatan and location of the 32 investigated cenotes. Details of the num- bered cenotes can be found in Table 1. The light area represents the Geohydrological Reserve in Yucatan, while the dark area depicts the urban extension of the city of Merida.

tubes and 10 cm diameter hand nets. Habitat data (e.g., depth, temperature, collected in cavern or cave, position relative to halocline) at the collection site of each individual was recorded along with photographs and video-recordings of the observed crustaceans and their habitats. All crustaceans were individually placed into 70 or 96% ethanol containing tubes immediately after collection. All specimens were collected under the permits of the Secretaria de Medio Ambiente y Recursos Naturales (SEMARNAT/ SPGA/DGVS/05263/14; SEMARNAT/SPGA/DGVS/02068/17). The collected ma- terial was deposited in the Yucatan Colleccién de Crustaceos, Unidad Multidiscipli- naria de Docencia e Investigacion, Universidad Nacional Auténoma de México in Sisal (UNAM UMDY-Sisal), the Colleccién Nacional de Crustaceos, Instituto de Biologia, UNAM in Mexico City, or in the Collection of Crustaceans of the Hungarian Natural History Museum (HNHM), Budapest.

New distribution records of subterranean crustaceans from cenotes in Yucatan 25

Morphological analysis

Individuals were examined using a stereo-microscope. Specimens of thermosbae- naceans, stygiomysids, mysids, and amphipods were studied as follows: cleared and stained exoskeletons were dissected under a Leica M125 stereo microscope. The dissec- tions were then mounted on slides and examined using a Leica DM 1000 compound light microscope (Fiser et al. 2009; Angyal et al. 2015). For the identification of the collected material the following publications were used: Alvarez et al. 2005; Alvarez and Iliffe 2008; Angyal et al. 2018; Botosaneanu and Iliffe 1999, 2000, 2002, 2006; Bowman 1966, 1977; Bruce 1986; Creaser 1936; Hobbs and Hobbs 1976; Hobbs et al. 1977; Hobbs 1979; Holsinger 1977, 1990; Horwitz et al. 1995; Kallmeyer and Carpenter 1996; Lowry and Myers 2013; Meland et al. 2015; Pérez-Aranda 1983a, 1983b, 1984a, 1984b; Tinnizi and Quddusi 1993; Wagner 1994. Photographs were made using an OMAX 14 OMP digital USB microscope camera, a Nikon D5300, and a Nikon D7000 with 60 mm macro lens.

Molecular studies (COI barcode sequences)

DNA extraction of the peracarids studied was performed using QlAamp DNA Microkit (QIAGEN), following the manufacturer's instructions. A few pereopods of each animal provided the necessary material to extract DNA. For PCR amplification of mitochon- drial COI, we used the primer pair LCO 1490 and HCO 2198 (Folmer et al. 1994). PCR reactions (25 pl) contained 13.85 pl mQ water, 2.5 pl 10x PCR buffer, 2.5 ul dNTP mix (2mM), 1.5 pl of each primers (5uM), 0.15 pl Fermentas Dream Taq (5U/ ul), and 3 pl DNA extract. PCR temperature conditions were set as follows: initial de- naturation for 3 min at 94 °C, denaturation for 45 sec at 94 °C, hybridization for 45 sec at 48 °C, and polymerization for 1 min at 72 °C. After thirty cycles, a final extension for 3 min at 72 °C was performed. PCR products were purified using Exo SAP-IT Express PCR Product Cleanup (Affymetrix) according to the manufacturer's instructions. The fragments were sequenced in both directions using PCR amplification primers with an ABI 3130 sequencer. Contigs were assembled and sequences were edited using BioEdit 7.1.11 sequence alignment editor software (Hall 1999): chromatograms of complement reverse and forward strings were compared, gaps were eliminated, while indels and stop codons were checked. 605-651 bp COI barcode sequences have been uploaded to the NCBI GenBank database. Accession numbers and localities are listed in Table 2.

Results

A total of 14 stygobiont crustacean species, belonging to six Malacostraca orders, was collected (Figures 2, 3). New records of each species at each cenote were assessed after an exhaustive literature investigation (Table 3). This evaluation was based only on the

26 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

Table 2. Locality data and GenBank accession number of COI gene fragments of one individual of each

newly collected stygobiotic peracarid species.

Taxon Locality Voucher GenBank Cited in (cenote) accession nr. Tulumella unidens (Thermosbaenacea) Sabtun 1 YUC-CC-255-11-004-656 MK900685 present study Stygiomysis cokei (Stygiomysida) Dzonotila | YUC-CC-255-11-004-638 MK900690 present study Stygiomysis cf. holthuisi (Stygiomysida) MK900689 present study Antromysis cenotensis (Mysida) MK981568 present study Mayaweckelia troglomorpha (Amphipoda) MF589977 Angyal et al. 2018 Mayaweckelia cenoticola (Amphipoda) Ayun-Nah | YUC-CC-255-11-003923 MF589975 Angyal et al. 2018 Tuluweckelia cernua (Amphipoda) Kankirixche | YUC-CC-255-11-003924 MF589983 Angyal et al. 2018 Creaseriella anops (Isopoda) Tza Itza HNHM-YUC_Isopoda-01 MK900687 present study Yucatalana robustispina (Isopoda) Kankirixche | YUC-CC-255-11-004-715 MK900686 present study Cirolana yunca (Isopoda) Tres Oches | HNHM-YUC-Isopoda-02 MK900688 present study

Table 3. Records of stygobiotic crustacean species collected between May 2016 and January 2018 in

32 cenotes of Yucatan. Bold-faced locality names represent new records for the cenote, while bold-faced

locality names with an asterisk (*) represent new records for the state of Yucatan.

Taxon THERMOSBAENACEA

Cenote

Tulumella unidens Bowman & Iliffe, 1988

Cervera*, Sabtun 1*

STYGIOMYSIDA Stygiomysis cokei Kallmeyer & Carpenther, 1996 Stygiomysis cf. holthuisi (Gordon, 1958)

MYSIDA

Antromysis cenotensis Creaser, 1936

AMPHIPODA Mayaweckelia cenoticola Holsinger, 1977 Mayaweckelia troglomorpha Angyal, 2018

Tres Oches, San Elias, Dzonotila, Yax-Kis Tres Oches, Tza Itza, X-Batun, Kanun, Kankirixche, Kakuel, Santito, Pol Box, Kankal, Flor de Liz, Bebelchen, Chihuo Hol, Yax Kis

Tza Itza, Dzonbakal, Nayah, Kampepen, Kanun, Xaan, Kakuel, Kankirixche, Santito, Pol Box, Kankal, Dzonotila, Ixim Ha, Noh’Chunck, X’kokob, Flor de Liz, Pixton, Bebelchen, El Virgen, Chihuo Hol

Ayun-Nah, Dzonotila, Ixim Ha, Bebelchen Dzonbakal*, Kanun*, Xaan*, Kankirixche*, Dzonotila*, X’kokob*, Chihuo Hol*, Yax-Kis*

Tuluweckelia cernua Holsinger, 1990

ISOPODA Creaseriella anops (Creaser, 1936) Yucatalana robustispina Botosaneanu & Iliffe, 1999

Cirolana yunca (Botosaneanu & Iliffe, 2000) DECAPODA

San Juan*, Dzonbakal*, Tres Oches*, Xaan*, Kakuel*, Kankirixche’*, Santito*, X’baba*, Sabtun 1*, Pixton*, Yax-Kis*

San Juan, Cervera, Tza Itza, Tres Oches, Kankirixche, Chihuo Hol Xaan, Kakuel, Kankirixche, Yaal Utsil, Tza Itza, Pol Box, Dzonotila, Xbaba, El Virgen, Chihuo Hol, Yax Kis

Tres Oches, X’baba, Chihuo Hol

Typhlatya dzilamensis Alvarez, Iliffe & Villalobos, 2005

Cervera, Sabtun 1

Typhlatya mitchelli Hobbs & Hobbs, 1976

San Juan, Tza Itza, Dzonbakal, Kampepen, Ayun-Nah, Tres Oches, Kakuel, Kankirixche, Sabtun 1, Bebelchen, El Virgen, Chihuo Hol

Typhlatya pearsei Creaser, 1936 Creaseria morleyi (Creaser, 1936)

Tres Oches, Xaan, Kankirixche, Nohmozon Tza Itza, Kampepen, Kakuel, Kankirixche, Santito, Kankal, Bebelchen, El Virgen, Dzalbay

collected material that has been deposited in scientific collections. Additional data based on observations, however, are mentioned in the “Remarks” section in each case.

An individual account for each species is subsequently discussed. 605-651 base-pair COI barcode sequences of the analyzed species (Table 2) were obtained and uploaded to NCBI GenBank (https://www.ncbi.nlm.nih.gov/genbank/).

New distribution records of subterranean crustaceans from cenotes in Yucatan 27

Subphylum: Crustacea

Class: Malacostraca Superorder: Peracarida Order: Thermosbaenacea Family: Tulumellidae

Tulumella unidens Bowman & Iliffe, 1988 Figure 2A

Material examined. 4 individuals; Cenote Cervera, depth 25.6-26.2 m, cave, in hy- drogen sulfide layer, around and below halocline, 26 °C, Yalsihom, Yucatan, Mexico; 8 May 2016; colls. D. Angyal & E. Chavez Solis. 4 individuals; Cenote Sabtun 1, depth 24.0-25.0 m, cavern, above and around halocline, 25 °C, Chunchumil, Yucatan, Mexico; 10 December 2017; colls. D. Angyal, E. Chavez Solis, S. Drs, Q. Hernandez & S. Reyes.

Previous distribution. Iliffe 1992; Iliffe 1993; Bowman and Iliffe 1988; Rocha et al. 1998; Pohlman et al. 2000; Pesce and Iliffe 2002; Alvarez et al. 2015; Olesen et al 2015; Benitez et al. 2019.

Type locality is Cenote Naharon (Cristal) in Quintana Roo. This species had only been reported from Quintana Roo from cenotes Calavera (Temple of Doom), Mayan Blue, Actun Ha (Carwash), Muknal, Naach Wennen Ha, Bang, Odyssey, Tabano, and Quebrada.

Remarks. Our findings extend the distribution area of this thermosbaenacean, previously endemic to Quintana Roo, to the cenotes located in the coastal areas north of Dzilam de Bravo and the east of Celestun. It is most likely that this species has a coastal distribution along the anchialine systems of the Yucatan Peninsula. Previous records were reported from cenotes located 2-10 km from the coastline near Tulum, where they occurred mostly above and at the halocline (Alvarez & Iliffe 2008; Alvarez et al. 2015; Benitez et al. 2019). In Cenote Cervera, 3.6 km inland from the northern coast of the Yucatan Peninsula, we observed individuals both above and below the halocline, as well as in the hydrogen sulfide layer.

Order: Stygiomysida Family: Stygiomysidae

Stygiomysis cokei Kallmeyer & Carpenther, 1996 Figure 2B

Material examined. | individual; Cenote Tres Oches, depth 21.6 m, cave, freshwater, 27 °C, Homun, Yucatan, Mexico; 5 June 2016; colls. D. Angyal & E. Chavez Solis. 2 individuals, Cenote San Elias, depth 28.2 m and 32.0 m, cavern, freshwater, 26

28 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

Figure 2. A Tulumella unidens (Thermosbaenacea) B Stygiomysis cokei (Stygiomysida) © Stygiomysis cf. holthuisi (Stygiomysida) D Antromysis cenotensis (Mysida) E Mayaweckelia troglomorpha (Amphipoda) F Mayaweckelia cenoticola (Amphipoda) G Tuluweckelia cernua (Amphipoda). Scale bars: 1 mm (A, C, D, F, G); 10 mm (B, E).

New distribution records of subterranean crustaceans from cenotes in Yucatan 29

°C, Homun, Yucatan, Mexico; 19 November 2017; colls. D. Angyal, E. Chavez Solis, S. Drs & L. Liévano. 2 individuals; Dzonotila, depth 20.8 m and 28.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 20 November 2017; colls. D. Angyal, E. Chavez Solis, S. Drs & B. Magafia. 1 individual; Yax-Kis, depth 12.1 m and 27.0 m, cave, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 27 January 2018; colls. D. Angyal, S. Drs & L. Liévano.

Previous distribution. Kallmeyer and Carpenter 1996; Pesce and Iliffe 2002; Alvarez and Iliffe 2008; Alvarez et al. 2015; Benitez et al. 2019.

Type locality is Cenote Calavera (Temple of Doom) in Quintana Roo. Further known localities in Quintana Roo are cenotes Mayan Blue, Naharon (Cristal), Escon- dido, Actun Ha (Carwash), Actun Ko, Na’ach Wennen Ha, Muknal and Tabano. From Yucatan the species was known from cenotes Papakal, San Eduardo, Kankirixche, Yaal Utsil and Dzonotila.

Remarks. Our records show that this species is distributed in cenotes of central Yu- catan and along the Ring of Cenotes. Among the two Stygiomysis species of the region, S. cokei proved to be rarer than Stygiomysis cf. holthuisi. New occurrences were recoded between 12-32 m deep in freshwater. In cenotes San Elias, Dzonotila and Yax-Kis it co- occurred with S. cf. holthuisi. Previously the species had also been reported in brackish habitats (Alvarez and Iliffe 2008; Alvarez et al. 2015).

Stygiomysis cf. holthuisi (Gordon, 1958) Figure 2C

Material examined. 2 individuals; Cenote Tres Oches, depth 21.6 m, cave, freshwater, 27 °C, Homun, Yucatan, Mexico; 5 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Tza Itza, depth 18.9 m, cavern, freshwater, 27 °C, Tecoh, Yucatan, Mexico; 10 May 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote X- Batun, depth 19.3 m, cavern, freshwater, 27 °C, San Antonio Mulix, Yucatan, Mexico; 14 May 2016; colls. R. Acosta, D. Angyal, J. Baduy & S. Reyes. 3 individuals; Cenote Kanun, depth 10.9-13.0 m, cave, freshwater, 26 °C, Homun, Yucatan, Mexico; 4 June 2016; colls. R. Acosta, D. Angyal, J. Baduy, B. Magafa & S. Reyes. 1 individual; Cenote Kakuel, depth 29.8 m, cave, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 10 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Kankirixche, depth 3 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 11 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Santito, depth 5.4 m, cavern, freshwater, 27 °C, Kopoma, Yucatan, Mexico; 10 November 2017; colls. D. Angyal, D. Drs & L. Liévano. 1 individual; Cenote Pol Box, depth 3.0 m, cavern, freshwater, 27 °C, Chochola, Yucatan, Mexico; 12 November 2017; colls. D. Angyal, S. Drs, L. Liévano & E. Sosa. 4 individuals; Cenote Kankal, depth 6.0-27.0 m, cavern, fresh- water, 25 °C, Homun, Yucatan, Mexico; 12 November 2017; colls. D. Angyal, S. Drs, L. Liévano & E. Sosa. 2 individuals; Cenote Flor de Liz, depth 3.0 m, cavern, freshwater, 27 °C, Tixkokob, Yucatan, Mexico; 17 December 2017; colls. D. Angyal,

30 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

S. Drs, L. Liévano & S. Reyes. 1 individual; Cenote Bebelchen, depth 30.0 m, cavern, freshwater, 25 °C, Sanahcat, Yucatan, Mexico; 18 December 2017; colls. D. Angyal, S. Drs, L. Liévano & S. Reyes. 2 individuals; Cenote Chihuo Hol, depth 16.0 and 25.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 26 January 2018; colls. D. Angyal, S. Drs, L. Liévano, B. Magafa & N. Simoes. 3 individuals; Yax Kis, depth 9.0-25.0 m, cave, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 27 January 2018; colls. D. Angyal, S. Drs & L. Liévano.

Previous distribution. Gordon 1958; Botosaneanu 1980; Bowman et al. 1984; Pesce and Iliffe 2002; Alvarez and Iliffe 2008, Alvarez et al. 2015, Benitez et al. 2019.

Type locality is Devil's Hole, St. Martin, Lesser Antilles (France). The species is known from the Bahamas, Anguilla, Puerto Rico, and the Yucatan Peninsula. In Quin- tana Roo S. cf. holthuisi was recorded from cenotes Mayan Blue, Casa Cenote, Na’ach Wennen Ha, Bang, Odyssey, Muknal, and Tabano. From Yucatan the species was pre- viously known only from a single locality, Cenote Mucuyche.

Remarks. We have also recorded the species from cenotes Yaal Utsil, San Elias, and Dzonotila in freshwater bodies in both cavern and cave sections, between 3 and 30 m deep. Alvarez and Iliffe (2008) and Alvarez et al. (2015) reported observations in both freshwater and around the halocline from cenotes in Quintana Roo.

Order: Mysida Family: Mysidae

Antromysis cenotensis Creaser, 1936 Figure 2D

Material examined. 21 individuals; Cenote Tza Itza, depth 12.7-13.5 m, cavern, freshwater, 27 °C, Tecoh, Yucatan, Mexico; 10 May 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Dzonbakal, depth 25.3 m, cavern, freshwater, 27 °C, San Antonio Mulix, Yucatan, Mexico; 14 May 2016; colls. R. Acosta, D. Angyal, J. Baduy & S. Reyes. 1 individual; Cenote Nayah, depth 27.9 m, entrance of cave part, freshwa- ter, 26 °C, Pixyah, Yucatan, Mexico; 17 May 2016; colls. D. Angyal & B. Magafia. 3 in- dividuals; Cenote Kampepen, depth 9.3-12.5 m, cavern, freshwater, 27 °C, Chinquila, Yucatan, Mexico; 17 May 2016; colls. D. Angyal & B. Magafa. 4 individuals; Cenote Kanun, depth 0.5 m, cenote entrance, freshwater, 26 °C, Homun, Yucatan, Mexico; 4 June 2016; colls. R. Acosta, D. Angyal, J. Baduy, B. Magafa & S. Reyes. 4 individuals; Cenote Xaan, depth 22.2-24.2 m, cavern and cave, freshwater, 27 °C, Homun, Yu- catan, Mexico; 9 June 2016; colls. D. Angyal & E. Chavez Solis. 15 individuals; Cenote Kakuel, depth 7.2-10.8 m, cavern, freshwater, 27 °C, Homun, Yucatan, Mexico; 10 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Kankirixche, depth 9.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 11 June 2016;

New distribution records of subterranean crustaceans from cenotes in Yucatan 31

colls. D. Angyal & E. Chavez Solis. 4 individuals; Cenote Kankirixche, depth 10.0- 25.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 25 January 2018; colls. D. Angyal, S. Drs, B. Magafa & L. Liévano. 18 individuals; Cenote Santito, depth 0.2-1.0 m, cavern, freshwater, 27 °C, Kopoma, Yucatan, Mexico; 10 November 2017; colls. D. Angyal, S. Drs & L. Liévano. 17 individuals; Cenote Pol Box, depth 5.2-9.3 m, cavern, freshwater, 27 °C, Chochola, Yucatan, Mexico; 12 November 2017; colls. D. Angyal, S. Drs, L. Liévano & E. Sosa. 1 individual; Cenote Kankal, depth 24.6 m, cavern, freshwater, 25 °C, Homun, Yucatan, Mexico; 18 November 2017; colls. D. Angyal, E. Chavez Solis, S. Drs & L. Liévano. 21 individuals; Dzonotila, depth 3.0- 27.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 20 November 2017; colls. D. Angyal, E. Chavez Solis, S. Drs & B. Magania. 5 individuals; Cenote Ixim Ha, depth 10.0 m, cavern, freshwater, 25 °C, Tixkakal, Yucatan, Mexico; 25 November 2017; colls. D. Angyal, E. Chavez Solis, S. Drs, L. Liévano & E. Sosa. 1 individual; Cenote Noh’Chunck, depth 12.0 m, cavern, freshwater, 25 °C, Chunchumil, Yucatan, Mexico; 25 November 2017; colls. D. Angyal, E. Chavez Solis, S. Drs, Q. Hernandez & S. Reyes. 11 individuals; Cenote X’kokob, depth 1.0-4.0 m, cavern, freshwater, 25 °C, Ekmul, Yucatan, Mexico; 17 December 2017; colls. D. Angyal, S. Drs, L. Liévano & S. Reyes. 14 individuals; Cenote Flor de Liz, depth 0.3-3.0 m, cavern, freshwater, 27 °C, Tixkokob, Yucatan, Mexico; 17 December 2017; colls. D. Angyal, S. Drs, L. Liévano & S. Reyes. 19 individuals; Cenote Pixton, depth 3.0 m, cavern, freshwater, 27 °C, Huhi, Yucatan, Mexico; 18 December 2017; colls. D. Angyal & L. Liévano. 11 individuals; Cenote Bebelchen, depth 27.0 m, cavern, freshwater, 25 °C, Sanahcat, Yucatan, Mexico; 18 December 2017; colls. D. Angyal, L. Liévano & S. Reyes. 6 indi- viduals; Cenote El Virgen, depth 25.0 m, cavern, freshwater, 26 °C, Sotuta, Yucatan, Mexico; 20 December 2017; colls. L. Liévano & N. Simoes. 3 individuals; Cenote Chihuo Hol, depth 11.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 20 December 2017; colls. D. Angyal, S. Drs, B. Magania, L. Liévano & N. Simoes.

Previous distribution. Creaser 1936, 1938; Nicholas 1962; Bowman 1977; Reddell 1977, 1981; Holsinger 1990; Iliffe 1992, 1993; Fiers et al. 1996; Rocha et al. 1998, 2000; Sudrez-Morales and Rivera Arriaga 1998; Pohlman et al. 2000; Pesce and Iliffe 2002; Schmitter-Soto et al. 2002; Alvarez and Iliffe 2008; Alvarez et al. 2015; Benitez et al. 2019.

Type locality is Grutas de Balankanche (Yucatan). Widely distributed in the central and northern parts of the Yucatan Peninsula, known from several wells, cenotes and caves of Quintana Roo and Yucatan.

Remarks. Antromysis cenotensis was present in all the cenotes studied, except for Cenote Cervera. Alvarez et al. (2015) mentions that A. cenotensis occurs mostly above or occasionally below the halocline up to a depth of 16 m. In the present study, the spe- cies was only observed in freshwater habitats, in some cases as deep as the scope of the survey. Our findings prove this species as a common representative of the stygofauna of Yucatan, as it was found in more than 95% of the visited sites. Antromysis cenotensis is listed as “threatened” in the Mexican Red List of Threatened Species (NOM-059 SEMARNAT 2010).

32 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

Order: Amphipoda Family: Hadziidae

Mayaweckelia troglomorpha Angyal, 2018 Figure 2E

Material examined. 2 individuals; Dzonbakal, depth 26.3 and 26.5 m, cave, fresh- water, 27 °C, San Antonio Mulix, Yucatan, Mexico; 14 May 2016; colls. R. Acosta, D. Angyal, J. Baduy & S. Reyes. 1 individual; Cenote Kanun, depth 24.3 m, cave, freshwater, 26 °C, Homun, Yucatan, Mexico; 4 June 2016; colls. R. Acosta, D. An- gyal, J. Baduy, B. Magafa & S. Reyes. 1 individual; Cenote Xaan, depth 25.4 m, cave, freshwater, 27 °C, Homun, Yucatan, Mexico; 9 June 2016; colls. D. Angyal & E. Chavez Solis. 2 individuals; Cenote Kankirixche, depth 20.4 and 33.3 m, cavern and cave, freshwater, 27 °C, Homun, Yucatan, Mexico; 11 June 2016; colls. D. Angyal & E. Chavez Solis. 5 individuals; Dzonotila, depth 11.0-17.7 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 20 November 2017; colls. D. Angyal, E. Chavez Solis, S. Drs & B. Magana. 2 individuals; Cenote X’kokob, depth 4.0-10.0 m, cavern, freshwater, 26 °C, Ekmul, Yucatan, Mexico; 17 December 2017; colls. D. Angyal, E. Chavez Solis, S. Drs & B. Magafia. 2 individuals; Cenote Chihuo Hol, depth 8.0- 27.2 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 26 January 2018; colls. D. Angyal, S. Drs, L. Liévano, B. Magafa & N. Simoes. 1 individual; Cenote Yax-Kis, depth 8.0 m, cave, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 27 Janu- ary 2018; colls. D. Angyal, S. Drs & L. Liévano.

Previous distribution. Angyal et al. 2018. Type locality is Dzonbakal (Yucat- an. Allotype female is from Cenote Kankirixche, paratypes are from Dzonbakal and cenotes Kanun, Xaan and Kankirixche (all in Yucatan).

Remarks. At present, collected material is available from eight localities and a small M. troglomorpha population was also observed in Cenote San Elias. All the in- dividuals were found in freshwater habitats, both in cave and cavern sections, where water temperature was between 26 and 27 °C. In cenote Kankirixche, some individu- als were observed below 45 meters in depth. As a species recently described by our research group, one of the outcomes of present expeditions. As M. troglomorpha was found in approximately 30% of the visited sites, it does not appear to be a rare fresh- water stygobiotic element in the Yucatan cenotes.

Mayaweckelia cenoticola Holsinger, 1977 Figure 2F

Material examined. | individual; Cenote Ayun-Nah, depth 14.0 m, cave, freshwater, 27 °C, Cacalchen, Yucatan, Mexico; 22 May 2016; colls. D. Angyal, B. Magafa & E. Sosa Rodriguez. 1 individual; Dzonotila, depth 18.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 20 November 2017; colls. D. Angyal. E. Chavez Solis, S.

New distribution records of subterranean crustaceans from cenotes in Yucatan 33

Drs & B. Magana. 1 individual; Cenote Ixim Ha, depth 4.7 m, cavern, freshwater, 25 °C, Tixkakal, Yucatan, Mexico; 25 November 2017; colls. D. Angyal, E. Chavez Solis, S. Drs, L. Liévano & E. Sosa. 3 individuals; Cenote Bebelchen, depth 0.5-7.3 m, cavern, freshwater, in water column and in roots at cavern entrance, 25 °C, Sanahcat, Yucatan, Mexico; 18 December 2017; colls. D. Angyal, S. Drs, L. Liévano & S. Reyes.

Previous distribution. Holsinger 1977, 1990; Reddell 1981; Alvarez and Iliffe 2008, Alvarez et al. 2015, Angyal et al. 2018, Benitez et al. 2019.

Type locality is Cenote Xtacabiha (Yucatan). From Yucatan the species was also known from Cueva de Orizaba, Cenote Nohchen, Grutas de Tzab-Nah and Grutas de Santa Maria. From Quintana Roo there were records from Cenote Actun Ha (Car- wash), Cenote de las Ruinas, Cenote de San Martin, Cenote de Santo Domingo, Cue- va de Tancah, Odyssey, Bang and Tabano. From the state of Campeche, the species was known from the Volcan de los Murciélagos cave.

Remarks. Mayaweckelia cenoticola proved to be rarer than M. troglomorpha, since it was recorded from only four cenotes. In Cenote Bebelchen we found some individuals in the roots of trees near the surface at the entrance region. Holsinger (1990) found that the species is associated mainly with freshwater habitats, with few populations oc- curring in weak brackish water. Individuals found in the Ox Bel Ha System (Quintana Roo) by Alvarez et al. (2015) and Benitez et al. (2019) also occurred in freshwater.

Tuluweckelia cernua Holsinger, 1990 Figure 2G

Material examined. 3 individuals; Cenote San Juan, depth 27.0-27.1 m, cave, fresh- water, 27 °C, Homun, Yucatan, Mexico; 7 May 2016; colls. D. Angyal & E. Chavez Solis. 2 individuals; Cenote Dzonbakal, depth 29.0 m, cave, freshwater, 27 °C, San Antonio Mulix, Yucatan, Mexico; 22 May 2016; colls. D. Angyal, J. Baduy & B. Magania. 10 individuals; Cenote Tres Oches, depth 15.8-22.9 m, cave, freshwater, 27 °C, Homun, Yucatan, Mexico; 5 June 2016; colls. D. Angyal & E. Chavez Solis. 3 individuals; Cenote Xaan, depth 22.7-26.6 m, cave, freshwater, 27 °C, Homun, Yu- catan, Mexico; 9 June 2016; colls. D. Angyal & E. Chavez Solis. 3 individuals; Cenote Kakuel, depth 32.2-38 m, cave, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 10 June 2016; colls. D. Angyal & E. Chavez Solis. 3 individuals; Cenote Kankirixche, depth 20.4-49.6 m, cavern and cave, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 11 June 2016; colls. D. Angyal & E. Chavez Solis. 2 individuals; Cenote Santito, depth 5.3-6.0 m, cavern, freshwater, 27 °C, Kopoma, Yucatan, Mexico; 10 November 2017; colls. D. Angyal, S. Drs & L. Liévano. 1 individual; Cenote X’baba, depth 26.0 m, cavern, freshwater, 27 °C, Chochola, Yucatan, Mexico; 26 November 2017; colls. S. Drs, L. Liévano & E. Sosa. 1 individual; Cenote Sabtun 1, depth 25.0 m, cavern, above the halocline, 25 °C, Chunchumil, Yucatan, Mexico; 10 December 2017; colls. D. Angyal, S. Drs, E. Chavez Solis, Q. Hernandez & S. Reyes. 1 individual; Cenote Pixton, depth 7.0 m, cavern, freshwater, 26 °C, Huhi, Yucatan, Mexico; 18 December

34 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

2017; colls. D. Angyal & L. Liévano. 3 individuals; Cenote Yax-Kis, depth 23.4-32.0 m, cave, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 27 January 2018; colls. D. Angyal, S. Drs & L. Liévano.

Previous distribution. Holsinger 1990; Alvarez and Iliffe 2008; Alvarez et al. 2015; Angyal et al. 2018; Benitez et al. 2019.

Type locality is Cenote Calavera (Temple of Doom) in Quintana Roo. This species was known only from coastal caves of Quintana Roo: Mayan Blue, Actun Ha (Car- wash), Mojara, Naharon (Cristal), Na’ach Wennen Ha, Bang, Muknal, Odyssey, and Tabano.

Remarks. Tiluweckelia cernua was both the most frequent and abundant stygo- biotic amphipod in the present study. Additional observations were from cenotes Yaal Utsil, El Virgen, and Dzalbay. In contrast with previous reports (e.g. Holsinger 1990), T. cernua always occurred in freshwater habitats. Individuals were collected between depths of 5-50 m. The species co-occurred with M. troglomorpha in five cenotes. These are the first distributional records of 7; cernua for the state of Yucatan. Known localities of this species have almost tripled, increasing its distribution range into the Yucatan inland area.

Order: Isopoda

Family: Cirolanidae

Creaseriella anops (Creaser, 1936) Figure 3A

Material examined. 3 individuals; Cenote San Juan, depth 20.0-28.0 m, cavern and cave, freshwater, 27 °C, Homun, Yucatan, Mexico; 7 May 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Cervera, depth 24.0 m, cave, below halocline, 26 °C, Yalsihom, Yucatan, Mexico; 8 May 2016; colls. D. Angyal & E. Chavez Solis. 2 individuals; Cenote Tza Itza, depth 12.5-13.5 m, cavern, freshwater, 27 °C, Te- coh, Yucatan, Mexico; 10 May 2016; colls. D. Angyal & E. Chavez Solis. 2 individu- als; Cenote Tres Oches, depth 18.2-21.7 m, cave, freshwater, 27 °C, Homun, Yu- catan, Mexico; 5 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Kankirixche, depth 3.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 11 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Chihuo Hol, depth 15.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 26 January 2018; colls. D. Angyal, S. Drs, L. Liévano, B. Magaha & N. Simoes.

Previous distribution. Creaser 1936, 1938; Nicholas 1962; Reddell 1977, 1981; Holsinger 1990; Iliffe 1992, 1993; Fiers et al. 1996; Rocha et al. 1998; Botosaneanu and Iliffe 1999, 2002; Alvarez et al. 2005; Iliffe and Botosaneanu 2006; Alvarez and Iliffe 2008; Sanchez-Rodriguez 2008; Ruiz-Cancino et al. 2013; Alvarez et al. 2015; Ortiz and Chazaro-Olvera 2015; Benitez et al. 2019.

New distribution records of subterranean crustaceans from cenotes in Yucatan 35

Type locality is Cenote Sambula (Motul, Yucatan). Known from numerous caves and cenotes in Quintana Roo and Yucatan, and a well in Campeche.

Remarks. The species was also observed in cenotes Yaal Utsil, Pol Box, X’kokob, Bebelchen, Kankal, San Elias, Dzonotila, Yax-Kis, Xaan and X’baba. Creaseriella anops was found both in cavern and cave sections, between 3 and 40 m deep. Our observa- tions generally agree with the records of Iliffe and Botosanenau (2006) and Alvarez et al. (2015) as a freshwater species. However, as Benitez et al. (2019) reported, we also ob- served individuals around or below the halocline. Creaseriella anops is listed as “threat-

ened” in the Mexican Red List of Threatened Species (NOM-059-SEMARNAT 2010).

Yucatalana robustispina Botosaneanu & Iliffe, 1999 Figure 3B

Material examined. | individual; Cenote Xaan, depth 27.6 m, cave, freshwater, 27 °C, Homun, Yucatan, Mexico; 9 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Kakuel, depth 19.9 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 10 June 2016; colls. D. Angyal & E. Chavez Solis. 5 individuals; Cenote Kankirixche, depth 20-49.3 m, cavern and cave, freshwater, 27 °C, Mucuy- che, Yucatan, Mexico; 11 June 2016; colls. D. Angyal & E. Chavez Solis. 3 individu- als; Cenote Kankirixche, depth 10.0-27.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 26 January 2018; colls. D. Angyal, S. Drs, L. Liévano & B. Magajfia. 1 individual; Cenote Yaal Utsil, depth 35.5 m, cave, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 3 November 2017; colls. D. Angyal, S. Drs & E. Chavez Solis. 1 individual; Cenote Tza Itza, depth 15.0 m, cavern, freshwater, 27 °C, Tecoh, Yu- catan, Mexico; 3 November 2017; colls. D. Angyal, S. Drs & L. Liévano. 1 individual; Cenote Pol Box, depth 3.0 m, cavern, freshwater, 27 °C, Chochola, Yucatan, Mexico; 12 November 2017; colls. D. Angyal, S. Drs, L. Liévano & E. Sosa. 2 individuals; Dzonotila, depth 14.0 and 16.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 12 November 2017; colls. D. Angyal, S. Drs, E. Chavez Solis & B. Magania. 1 individual; Cenote X’baba, depth 12.0 m, cave, freshwater, 25 °C, Chochola, Yu- catan, Mexico; 12 November 2017; colls. S. Drs, L. Liévano 8 E. Sosa. 1 individual; Cenote El Virgen, depth 12.6 m, cavern, freshwater, 26 °C, Sotuta, Yucatan, Mexico; 20 December 2017; colls. L. Liévano & N. Simoes. 1 individual; Cenote Chihuo Hol, depth 20.6 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 26 Janu- ary 2018; colls. D. Angyal, S. Drs, L. Liévano, B Magafia & N. Simoes. 3 individuals; Cenote Yax Kis, depth 12.0-33.0 m, cave, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 27 January 2018; colls. D. Angyal, S. Drs & L. Liévano.

Previous distribution. Botosaneanu and Iliffe 1999, 2002, 2006; Alvarez and II- iffe 2008.

Type locality is Cenote Pabakal (Papakal), Yucatan. It was also found in cenotes Kankirixche, Kakuel, Chuih-Hol Dos, Xacha, and San Geronimo (all in Yucatan).

36 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

Figure 3. A Creaseriella anops (Isopoda) B Yucatalana robustispina (Isopoda); C Cirolana yunca (Isopoda) D Zyphlatya dzilamensis (Decapoda) E Typhlatya mitchelli (Decapoda) F Typhlatya pearsei (Decapoda) G Creaseria morleyi (Decapoda). Scale bars: 1 mm (B, C, F); 10 mm (A, D, E, G).

New distribution records of subterranean crustaceans from cenotes in Yucatan 37

Remarks. Individuals of Y° robustispina were collected in a third of all locali- ties visited, where it occurred in freshwater between 3 and 49 m in depth. In eight cenotes Y. robustispina co-occurred with the isopod C. anops. Agreeing with our ob- servations, previous records referred specimens caught in freshwater between 5-50 m in depth (Botosaneanu and Iliffe 1999, 2002, 2006). Known localities of this species have been doubled.

Cirolana yunca (Botosaneanu & Iliffe, 2000) Figure 3C

Material examined. | individual; Cenote Tres Oches, depth 22.4 m, cave, freshwater, 27 °C, Homun, Yucatan, Mexico; 5 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote X’baba, depth 25.0 m, cave, freshwater, 25 °C, Chochola, Yucatan, Mexico; 26 November 2016; colls. S. Drs, L. Liévano & E. Sosa. 1 individual; Cenote Chihuo Hol, depth 19.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 26 January 2018; colls. D. Angyal, S. Drs, L. Liévano, B Magafa & N. Simoes. 1 individual.

Previous distribution. Botosaneanu and Iliffe 2000, 2006; Alvarez and Iliffe 2008; Rocha-Ramirez et al. 2009.

Type locality is Cenote Sabak Ha (Yucatan). This species had only been collected from its type locality until our expeditions.

Remarks. We here provide the first records after the original description, which was based on a single specimen collected at 60 m in depth near the halocline at a salinity of 1.4 g/l (Botosaneanu and Iliffe 2000, 2006). The three newly collected indi- viduals were found in freshwater habitats, both in cavern and cave zones below 19 m in depth. The species was found in approximately 10% of the studied cenotes always as solitary individuals. Therefore, C. yunca seems to be a rare element of the Yucatan freshwater cenote ecosystems.

Superorder: Eucarida Order: Decapoda Family: Atydae

Typhlatya dzilamensis Alvarez, Iliffe & Villalobos, 2005 Figure 3D

Material examined. | individual; Cenote Cervera, depth 27.4 m, cave, below halo- cline, 27 °C, Yalsihom, Yucatan, Mexico; 8 May 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Sabtun 1, depth 28 m, cavern, below halocline, 26 °C, Chunchumil, Yucatan, Mexico; 10 Dec 2017; colls. D. Angyal & E. Chavez.

Previous distribution. Alvarez et al. 2005, 2015; Alvarez and Iliffe 2008; Benitez et al. 2019; Espinasa et al. 2019.

38 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

Type locality is Buya Uno, allotype was collected from Cenote Cervera and para- types from Dzilamway, all cenotes in Dzilam de Bravo region (Yucatan north coast). This species was recently recorded at the Ox Bel Ha system south of Tulum (Benitez et al. 2019) and the Ponderosa system north of Tulum (Espinasa et al. 2019).

Remarks. In accordance with previous records by Alvarez et al. (2005, 2015), our specimens were also collected in fully marine water. Recent observations of this spe- cies increase the expected distribution, suggesting an underground coastal and saline habitat that could extend from the south of Quintana Roo (Ox Bel Ha) to the west coast of Yucatan (Sabtun 1).

Typhlatya mitchelli Hobbs & Hobbs, 1976 Figure 3E

Material examined. 3 individuals; Cenote San Juan, depth 4.3-9.1 m, cave and cav- ern, freshwater, 27 °C, Homun, Yucatan, Mexico; 7 May 2016; colls. D. Angyal & E. Chavez Solis. 11 individuals; Cenote Tza Itza, depth 4.3-16.5 m, cave, freshwater, 27 °C, Tecoh, Yucatan, Mexico; 10 May 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Dzonbakal, depth 9.3 m, cavern, freshwater, 27 °C, San Antonio Mulix, Yucatan, Mexico; 14 May 2016; colls. R. Acosta, D. Angyal, J. Baduy & S. Reyes. 1 individual; 1 individual; Cenote Dzonbakal, depth 14 m, cavern, fresh- water, 27 °C, San Antonio Mulix, Yucatan, Mexico; 29 May 2016; colls. D. Angyal, J. Baduy & B. Magafia. 5 individuals; Cenote Kampepen, depth 10.1 m, cavern, freshwater, 27 °C, Chinquila, Yucatan, Mexico; 17 May 2016; colls. D. Angyal & B. Magafia. 2 individuals; Cenote Ayun-Nah, depth 9 m, cave, freshwater, 27 °C, Cacalchen, Yucatan, Mexico; 22 May 2016; colls. D. Angyal, B. Magafa & E. Sosa Rodriguez. Cenote Tres Oches, depth 8.1-22 m, cave, freshwater, 27 °C, Homun, Yucatan, Mexico; 5 June 2016; colls. D. Angyal & E. Chavez Solis. 7 individuals; Cenote Kakuel, depth 5-25.8 m, cave and cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 10 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Kankirixche, depth 30.2 m, cavern, freshwater, 27 °C, Mucuyche, Yucat- an, Mexico; 10 December 2016; colls. D. Angyal & E. Chavez Solis. 2 individuals; Cenote Sabtun 1, depth 24.0 and 25.0 m, cavern, above the halocline, 25 °C, Chun- chumil, Yucatan, Mexico; 10 December 2017; colls. D. Angyal, E. Chavez Solis, S. Drs, Q. Hernandez & S. Reyes. 1 individual; Cenote Bebelchen, depth 34.0 m, cavern, freshwater, 25 °C, Sanahcat, Yucatan, Mexico; 18 December 2017; colls. D. Angyal, S. Drs, L. Liévano & S. Reyes. 1 individual; Cenote El Virgen, depth 19.9 m, cavern, freshwater, 26 °C, Sotuta, Yucatan, Mexico; 20 December 2017; colls. L. Liévano & N. Simoes. 1 individual; Cenote Chihuo Hol, depth 26.0 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 26 January 2018; colls. D. Angyal, S. Drs, B. Magana, L. Liévano & N. Simoes.

New distribution records of subterranean crustaceans from cenotes in Yucatan by

Previous distribution. Hobbs and Hobbs 1976; Hobbs et al. 1977; Hobbs 1979; Reddell 1977, 1981; Iliffe 1992; Rocha et al. 1998; Webb 2003; Botello and Alvarez 2013; Benitez 2014; Alvarez et al. 2015; Chavez Solis 2015; Benitez et al. 2019.

Type locality is Cenote Kabahchen (Yucatan). The species occurs in numerous caves and cenotes throughout the peninsula in Quintana Roo and Yucatan.

Remarks. Our findings corroborate that 7’ mitchelli is a widespread common crus- tacean in the freshwater cenotes of Yucatan. This species was caught from the shallow zones to 34 m in depth, indicating a wide vertical range as well as a wide geographical range. The species was also observed (but not collected) in cenotes Yaal Utsil, Santito, Pol Box, Kankal, San Elias, Dzonotila, X’baba, X’kokob, Pixton, Dzalbay, and Yax- Kis. Typhlatya mitchell: is listed as “least concern” in the IUCN Red List (De Grave et al. 2013a) and as “threatened” in the Mexican Red List of Threatened Species (NOM- 059-SEMARNAT 2010).

Typhlatya pearsei Creaser, 1936 Figure 3F

Material examined. | individual; Cenote Tres Oches, depth 21.6 m, cave, fresh- water, 27 °C, Homun, Yucatan, Mexico; 6 June 2016; colls. D. Angyal & E. Chavez Solis. 2 individuals; Cenote Xaan, depth 25.8 and 26.1 m, cave, freshwater, 27 °C, Homun, Yucatan, Mexico; 9 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individ- ual; Cenote Kankirixche, depth 3 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 11 June 2016; colls. D. Angyal & E. Chavez Solis. Cenote Nohmozon, depth 12.2 m, cavern, freshwater, 25 °C, Pixyah, Tecoh, Yucatan, Mexico; 11 March 2016; colls. E. Chavez Solis.

Previous distribution. Creaser 1936; Nicholas 1962; Hobbs et al. 1977; Holthuis 1977; Hobbs 1979; Reddell 1977, 1981; Pérez-Aranda 1983a; Holsinger 1990; Iliffe 1992; Webb 2003; Hunter et al. 2007; Yager and Madden 2010; Botello and Alvarez 2013; Mejia-Ortiz et al. 2013; Benitez 2014; Pakes et al. 2014; Alvarez et al. 2015; Chavez Solis 2015; Benitez et al. 2019.

Type locality is “Balam Canche Cave’ (Grutas de Balankanche, Yucatan). The spe- cies is widely distributed within the northern part of the Yucatan Peninsula; it occurs in Quintana Roo, Yucatan, and Campeche.

Remarks. Despite previous studies stating that 7’ pearsei has the largest of Ty- phlatya’s distribution range in the Yucatan Peninsula (Alvarez et al. 2015), we only collected individuals in a few localities, where it occurred in freshwater, both near the surface in open cenote pools and in deeper cave passages up to 26 m in depth. This species is listed as “least concern” in the IUCN Red List (De Grave et al. 2013b) and as “threatened” in the Mexican Red List of Threatened Species (NOM-059-SEMAR- NAT 2010).

40 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

Family: Palaemonidae

Creaseria morleyi (Creaser, 1936) Figure 3G

Material examined. 2 individuals; Cenote Tza Itza, depth 15.4 m, cavern, freshwater, 27 °C, Tecoh, Yucatan, Mexico; 10 May 2016; colls. D. Angyal & E. Chavez Solis. 2 individuals; Cenote Kampepen, depth 6-9.5 m, cavern, freshwater, 27 °C, Chinquila, Yucatan, Mexico; 17 May 2016; colls. D. Angyal & B. Magafia. 2 individuals; Cenote Kakuel, depth 3 and 13.9 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 10 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Kankirixche, depth 3.6 m, cavern, freshwater, 27 °C, Mucuyche, Yucatan, Mexico; 11 June 2016; colls. D. Angyal & E. Chavez Solis. 1 individual; Cenote Santito, depth 4.0 m, cavern, freshwater, 27 °C, Kopoma, Yucatan, Mexico; 10 November 2017; colls. D. Angyal, S. Drs & L. Liévano. 1 individual; Cenote Kankal, depth 0.3 m, cavern, freshwater, 25 °C, Homun, Yucatan, Mexico; 18 November 2017; colls. D. Angyal, S. Drs, E. Chavez Solis & L. Liévano. 1 individual; Cenote Bebelchen, depth 30.0 m, cavern, freshwater, 25 °C, Sanahcat, Yucatan, Mexico; 18 December 2017; colls. D. Angyal, L. Liévano & S. Reyes. 1 individual; Cenote El Virgen, depth 25.0 m, cavern, freshwater, 26 °C, Sotuta, Yucatan, Mexico; 20 December 2017; colls. L. Liévano & N. Simoes. 1 individual; Cenote Dzalbay, depth 4.3 m, cavern, freshwater, 23 °C, Sotuta, Yucatan, Mexico; 20 December 2017; colls. D. Angyal & L. Liévano.

Previous distribution. Creaser 1938; Hobbs and Hobbs 1976; Holthuis 1977; Hobbs et al. 1977; Reddell 1977, 1981; Hobbs 1979; Pérez-Aranda 1983b; Iliffe 1992: Botello and Alvarez 2006; Botello and Alvarez 2010; Benitez 2014; Alvarez et al. 2015; Chavez Solis 2015; Chavez Solis et al. 2017; Benitez et al. 2019.

Type locality is San Isidro Cave (Yucatan). Widely distributed in cenotes and caves of Yucatan, Campeche, and Quintana Roo.

Remarks. Reddell (1981) mentions the species as an “ever-present element of fauna of pools and lakes in caves in the Yucatan Peninsula’. In addition to the above listed localities, we also observed the species in cenotes Yaal Utsil, Pol Box, San Elias, Dzonotila, Flor de Liz, X’baba, Chihuo Hol, and Yax-Kis. Specimens were recorded in both cave and cavern sections, up to 38 m in depth. Benitez et al. (2019) also found individuals around and below the halocline in cenotes belonging to the Ox Bel Ha sys- tem. Creaseria morleyi is listed as “threatened” in the Mexican Red List of Threatened Species (NOM-059-SEMARNAT 2010) and as “least concern” in the IUCN Red List (De Grave et al. 2013c).

Discussion

While there are more than 3,000 registered cenotes in the state of Yucatan (SDS Yu- catan census), less than five percent have been zoologically investigated. Results herein confirm that the region deserves more attention and that the geographical, bathymet-

New distribution records of subterranean crustaceans from cenotes in Yucatan 4]

ric, and fresh/salt water distribution of stygobiotic species is far from being fully under- stood. In order to contribute to the management of the vulnerable cenote ecosystems and their highly specialized endemic stygofauna, collecting as much information as possible about the biology of Yucatan aquifers would be paramount. This data should include reports on the species’ distribution, density and rarity, taxonomy, ecology, as well as characteristics of their habitats related to their biology, such as the amount of epigean originated organic sources or the degree of anthropogenic pollution in cenotes.

Prior to this study, the amphipod 7 cernua was only known from Quintana Roo, mostly associated with saltwater habitats in anchialine cenotes near the northeastern coastline of the Peninsula (Holsinger 1990; Rocha et al. 1998; Alvarez and Iliffe 2008; Alvarez et al. 2015). Contrary to previous findings, all individuals were found in fresh- water habitats during our study (Angyal et al. 2018). Rocha et al. (1998) and Pesce and Iliffe (2002) mentioned observation records of ’thermosbaenaceans’ from cenotes Yun- cu, Mucuyche, Pabakal (Papakal), and Grutas de Tzab-Nah (all in Yucatan). However, these individuals had never been identified at the species level and it seems no voucher information of the potentially collected specimens is available. The present study con- firms first records for 7’ cernua and T. unidens in the state of Yucatan. Together with the amphipod M. troglomorpha, which was discovered and described within the frame of herein presented expeditions (Angyal et al. 2018) and the new cave isopod Curas- santhura yucatanensis Alvarez, Benitez, Iliffe & Villalobos, 2019 (Alvarez et al. 2019), the list of stygobiotic crustaceans recorded for the state of Yucatan raised from 22 (in 2016) to 26. In addition, the cirolanid isopod C. yunca was only known from its type locality, but we now provide distribution data for this species in three other localities. Our results show that the stygiomysid S. cf. olthuisi has historically been unrecogniz- ed, unsampled or ignored. This specific contribution proves that inland cenotes have been understudied and distribution patterns of stygofauna are still unknown. Due to the previously lacking zoological information for the vast majority of the cenotes inves- tigated in our study, most of the distribution records presented here are new.

A closer morphological and molecular analysis of the Zyph/atya species in Yucatan is recommended in order to distinguish cryptic species that may be causing confound- ing biodiversity and ecological patterns in the Yucatan Peninsula.

Among the 14 crustacean species listed, prior to this study, cytochrome c oxidase subunit I sequences were publicly available only for the decapods 7’ mitchelli, T’ pearsei, LT. dzilamensis, and C. morleyi. The currently published COI barcode gene fragments can aid future molecular research on the peracarid fauna of Yucatan’s cenote ecosystems by facilitating their identification, as well as in the recognition of cryptic species.

The mysid A. cenotensis, the atyid shrimps 7’ mitchelli and T! pearsei and the pal- aemonid shrimp C. morleyi are listed in the Mexican and IUCN red lists of threatened species (SEMARNAT 2010; De Grave et al. 2013a, b, c). These species are present in most cenotes throughout the Yucatan Peninsula and can be considered a selected group of species whose protection will act as an umbrella in protecting other less common ones. On the other hand, there are rare species with an extremely narrow distribution range, which are not yet under legal protection. This makes these species even more vulnerable to urbanization and environment deterioration. Therefore, we suggest the

42 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

inclusion of narrow endemic species into the national and international protection lists, such as the isopod C. yunca or the atyid shrimp 7’ dzilamensis.

The number of new records provided in this work shows a historic lack of biodi- versity surveys in underwater caves of inland cenotes of the state of Yucatan. Most of the biodiversity and its distribution patterns are currently biased towards large popula- tions, easily accessible sites, and touristic attractions. Our efforts yield a greater under- standing of the distribution patterns of stygofauna in Yucatan cenotes.

Acknowledgements

We are grateful to Sophia Drs (Van Hall Larenstein University of Applied Sciences) for her support during the field trips and for her contribution in compiling cenote biodi- versity databases. Silvia Reyes, Quetzali Hernandez, Juan Baduy Infante, Rafael Acosta, Cristian Selin, Nori Velazquez Juarez, Jonathan Mondragon, Ricardo Riestra, Lorenzo Ortiz, Erick Sosa Rodriguez, and the Ecologistas sub-acuaticos de Yucatan (Subaquatic Ecologists of Yucatan) are greatly acknowledged for their assistance during the field trips and cave dives. Isaac Chacén and Ricardo Riestra (UNAM) are acknowledged for the information collected in the cenote databases. We thank Sergio Rodriguez Morales (UNAM) for providing facilities of the Chemistry Laboratory during the pretreat- ment of the dissected individuals. Virag Krizsik (HNHM, Laboratory of Molecular Taxonomy) is acknowledged for her professional help provided in molecular studies. We are grateful to Alberto Guerra (Nature Art) for making the photo tables. We thank Laszlo Danyi (HNHM, Department of Zoology) for the photograph of C. yunca. We would like to express our deep gratitude to the reviewers Thomas Iliffe (Texas A&M University of Galveston) and Alejandro Martinez (Italian National Research Council) for their useful suggestions, which helped us to improve the manuscript. DA is thank- ful for the scholarship received from “DGAPA-UNAM Programa de Becas Posdocto- rales en la UNAM, 2019”. ECS is grateful for the scholarship received from CONA- CyT 545277/294499 through “Posgrado en Ciencias Bioldégicas” of the UNAM. LLB gratefully acknowledges the scholarship provided by CONACyT 864025/628560 through “Posgrado en Ciencias del Mar y Limnologia’ of the UNAM. Financial sup- port was provided by project PAPITT IN222716 "Biodiversidad y Ecologia de la fauna de cenotes de Yucatan" and “Hacifa un mapa de biodiversidad acuatica de cenotes de la

Peninsula de Yucatan”, DGAPA-PAPIIT 2019 — IN228319 to NS.

References

Alvarez F, lliffe TM, Villalobos JL (2005) New species of the genus Typhlatya (Decapoda: Atyi- dae) from anchialine caves in Mexico, the Bahamas and Honduras. Journal of Crustacean

Biology 25(1): 81-94. https://doi.org/10.1651/C-2516

New distribution records of subterranean crustaceans from cenotes in Yucatan 43

Alvarez F, Iliffe TM (2008) Fauna anquihalina de Yucatan. In: Alvarez F, Rodriguez-Almaraz R (Eds) Crustaceos de Mexico: Estado Actual de su Conocimiento. Universidad Aut6noma de Nuevo Leén-PROMEP, 379-418.

Alvarez F, Iliffe TM, Benitez S$, Brankovits D, Villalobos JL (2015) New records of anchia- line fauna from the Yucatan Peninsula, Mexico. Check List 11(1): 1505. https://doi. org/10.15560/11.1.1505

Alvarez F, Benitez S, Iliffe TM, Villalobos JL (2019) A new species of isopod of the genus Curassan- thura (Cymothoida, Anthuroide, Leptanthuridae) from anchialine caves of the Yuctan Pen- insul, Mexico. Crustaceana 92(5): 545-553. https://doi.org/10.1163/1685403-00003892

Angyal D, Balazs G, Zaksek V, Krizsik V, Fiser C (2015) Redescription of two subterranean amphipods Niphargus molnari Méhely, 1927 and Niphargus gebhardti Schellenberg, 1934 (Amphipoda, Niphargidae) and their phylogenetic position. ZooKeys 509: 53-85. https:// doi.org/10.3897/zookeys.509.9820

Angyal D, Chavez Solis EM, Magana B, Balazs G, Simoes N (2018) Mayaweckelia troglo- morpha, a new subterranean amphipod species from Yucatan State, Mexico (Amphipoda, Hadziidae). ZooKeys 735: 1-25. https://doi.org/10.3897/zookeys.735.21164

Bauer-Gottwein P, Gondwe BRN, Chauvert G, Marin LE, Rebolledo-Vieyra M, Merediz- Alonso G (2011) The Yucatan Peninsula karst aquifer, Mexico. Hydrogeology Journal 19(3): 507-524. https://doi.org/10.1007/s10040-010-0699-5

Benitez SA (2014) Variacién en la estructura y composicién de la fauna anquihalina del sistema Ox Bel Ha (peninsula de Yucatan) a través de un gradiente de distancia desde la zona lito- ral. MSc Thesis, Universidad Nacional Auténoma de Mexico, Mexico DE

Benitez S, Iliffe TM, Quiroz-Martinez B, Alvarez F (2019) How is the anchialine fauna distrib- uted within a cave? A study of the Ox Bel Ha System, Yucatan Peninsula, Mexico. Subter- ranean Biology 31: 15-28. https://doi.org/10.3897/subtbiol.3 1.34347

Bishop RE, Iliffe T (2009) Metabolic rates of stygobiontic invertebrates from the Tunel de la Atlantida, Lanzarote. Marine Biodiversity 39(3): 189-194. https://doi.org/10.1007/ s12526-009-0018-3

Bishop RE, Humphreys WE, Cukrov N, Zié V et al. (2015) ’Anchialine’ redefined as a subterra- nean estuary in a crevicular or cavernous geological setting. Journal of Crustacean Biology 35(4): 511-514. https://doi.org/10.1163/1937240x-00002335

Botello A, Alvarez F (2006) Allometric growth in Creaseria morleyi (Creaser, 1936) (Decapoda: Palaemonidae), from the Yucatan Peninsula, Mexico. Caribbean Journal of Science 42: 171-179.

Botello A, Alvarez F (2010) Genetic variation in the stygobitic shrimp Creaseria morleyi (De- capoda: Palaemonidae), evidence of bottlenecks and re-invasions in the Yucatan Penin- sula. Biological Journal of the Linnean Society 99(2): 315-325. https://doi.org/10.1111/ j.1095-8312.2009.01355.x

Botello A, Alvarez F (2013) Phylogenetic relationships among the freshwater genera of palae- monid shrimps (Crustacea: Decapoda) from Mexico, evidence of multiple invasions. Latin American Journal of Aquatic Research 41(4): 773-780. https://doi.10.3856/vol41-issue4- fulltext-14

44 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

Botosaneanu L (1980) Stygiomysis holthuisi found on Anguilla (Crustacea: Mysidacea). Studies on the Fauna of Curaacao and other Caribbean Islands 61(190): 128-132.

Botosaneanu L (1986) Stygofauna mundi: A Faunistic, Distributional, and Ecological Syn- thesis of the World Fauna inhabiting Subterranean Waters. Journal of Crustacean Biology 7(1): 203. https://doi.org/10.2307/1548640

Botosaneanu L, Iliffe TM (1999) On four new stygobitic cirolanids (Isopoda: Cirolanidae) and several already described species from Mexico and the Bahamas. Bulletin de I'Institute Royal des Sciences Naturelles de Belgique, Biologie 69: 93-123.

Botosaneanu L, Iliffe TM (2000) Two new stygobitic species of Cirolanidae (Isopoda) from deep cenotes in Yucatan. Bulletin de l'Institute Royal des Sciences Naturelles de Belgique, Biologie 70: 149-161. https://www.biotaxa.org/Zootaxa/article/view/zootaxa.1823.1.4

Botosaneanu L, Iliffe TM (2002) Stygobitic isopod crustaceans, already described or new, from Bermuda, the Bahamas, and Mexico. Bulletin de l'Institut Royal des Sciences Naturelles de Bel- gique, Biologie 72: 101-111. https://www.tamug.edu/cavebiology/reprints/Reprint-139.pdf

Botosaneanu L, Iliffe TM (2006) The remarkable diversity of subterranean Cirolanidae (Crus- tacea: Isopoda) int he peri-Carribean and Mexican Realm. Bulletin de I'Institute Royal des Sciences Naturelles de Belgique, Biologie 76: 5—26. http://biblio.naturalsciences.be/rbins- publications/bulletin-of-the-royal-belgian-institute-of-natural-sciences-biologie/76-2006/ biologie-2006-76_5-26.pdf

Bowman TE (1966) Cirolana trichostoma, a new genus and species of troglobitic cirola- nid isopod from Cuba. International Journal of Speleology 2: 105-108. https://doi. org/10.5038/1827-806X.2.1.8

Bowman TE (1977) A review of the genus Antromysis (Crustacea: Mysidacea), including new species from Jamaica and Oaxaca, Mexico, and a redescription and new records for A. cenotensis. In: Reddell J (Ed) Studies on the caves and cave fauna of the Yucatan Peninsula. Association for Mexican Cave Studies Bulletin 6: 27—38.

Bowman TE, Iliffe TM, Yager J (1984) New records of the troglobitic mysid genus Stygiomysis: S. clarkei, new species, from the Caicos Islands, and S. holthuisi (Gordon) from Grand Ba- hama Island (Crustacea: Mysidacea). Proceedings of the Biological Society of Washington 97: 637-644. https://biodiversitylibrary.org/page/34642466

Bowman TE, Iliffe TM (1988) Tulumella unidens, a new genus and species of thermosbae- nacean crustacean from the Yucatan Peninsula, Mexico. Proceedings of the Biological Soci- ety of Washington 101: 221-226. http://biodiversitylibrary.org/page/34645902

Bruce NL (1986) Cirolanidae (Crustacea: Isopoda) of Australia. Records of the Australian Mu- seum, Supplement 6. The Australian Museum, Sydney, 239 pp. https://journals.australian- museum. net.au/bruce-1986-rec-aust-mus-suppl-6-1239/

Chavez Solis EM (2015) Aspectos ecoldgicos y etolégicos de decapodos estigobios (Creaseria morleyi y Typhlatya spp.) en cenotes de Yucatan: utilizatcidn espaciotemporal, cambios anuales y relaciones interespecificas. MSc Thesis, Mexico D. F., Mexico: Universidad Na- cional Auténoma de Mexico.

Chavez Solis EM, Mejia-Ortiz L, Simoes N (2017) Predatory behavior of the cave shrimp Crea- seria morleyi(Creaser, 1936) (Caridea: Palaemonidae), the blind hunter of the Yucatan ce- notes, Mexico. Journal of Crustacean Biology. 38. https://doi.org/10.1093/jcbiol/rux098

New distribution records of subterranean crustaceans from cenotes in Yucatan 45

Creaser EP (1936) Crustaceans from Yucatan, In: Pearse AS, Creaser EP, Hall FG (Eds): The Cenotes of Yucatan. Carnegie Institute of, Washington Publications 457: 117-132.

Creaser EP (1938) Larger cave crustacea of the Yucatan Peninsula. Carnegie Institute of Wash- ington Publications 491: 159-164.

De Grave S, Alvarez F, Villalobos J (2013a) Typhlatya mitchelli. The IUCN Red List of Threat- ened Species 2013: e.T197618A2493242. https://doi.org/10.2305/IUCN.UK.2013-1. RLTS.T197618A2493242.en [Downloaded on 23 December 2019]

De Grave S, Villalobos J, Alvarez F (2013b) Typhlatya pearsei. The IUCN Red List of Threat- ened Species 2013: e.T197616A2493158. https://doi.org/10.2305/IUCN.UK.2013-1. RLTS.T197616A2493158.en [Downloaded on 23 December 2019]

De Grave S, Alvarez FE, Villalobos J (2013c) Creaseria morleyi. The IUCN Red List of Threat- ened Species 2013: e.T198148A2513584. https://doi.org/10.2305/IUCN.UK.2013-1. RLTS.T198148A2513584.en [Downloaded on 23 December 2019]

Espinasa L, Chavez Solis EM, Mascaré M, Rosas C, Violette G (2019) A new locality and phy- logeny of the stygobitic Typh/atya shrimps for the Yucatan Peninsula. Speleobiology Notes 10: 19-27. https://doi.org/10.5563/spbn.v10i0.91

Fiers E, Reid JW, Iliffe TM, Suarez-Morales E (1996) New hypogean cyclopoid copepods (Crustacea) from the Yucatan Peninsula, Mexico. Contributions to Zoology 66(2): 65— 102. https://doi.org/10.1163/26660644-06602001

Fiser C, Trontelj P, Lustrik R, Sket B (2009) Towards a unified taxonomy of Niphargus (Crusta- cea: Amphipoda): a review of morphological variability. Zootaxa 2061: 1-22.

Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mo- lecular Marine Biology and Biotechnology 3: 294-299.

Gonzalez-Herrera R, Sanchez-Pinto I, Gamboa-Vargas J (2002) Groundwater-flow modeling in the Yucatan karstic aquifer, Mexico. Hydrogeology Journal 10(5): 539-552. https://doi. org/10.1007/s10040-002-0216-6

Gonzalez BC, Worsaae K, Fontaneto D (2018) Anophthalmia and elongation of body append- ages in cave scale worms (Annelida: Aphroditiformia). Zoologica Scripta 47(1):106-121. https://doi.org/10.1111/2sc.12258

Gordon I (1958) A new subterranean crustacean from the West Indies. Nature 181: 1552- 1553. https://doi.org/10.1038/1811552a0

Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis pro- gram for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98. https://doi. org/10.4236/sgr2.2015.64887

Hervant F, Mathieu J, Barré H (1999) Comparative study on the metabolic responses of sub- terranean and surface-dwelling amphipods to long-term starvation and subsequent refeed- ing. Journal of Experimental Biology 202: 3587-3595. https://jeb.biologists.org/con- tent/202/24/3587

Hervant F, Mathieu J, Durand J (2001) Behavioural, physiological and metabolic responses to long-term starvation and refeeding in a blind cave-dwelling (Proteus anguinus) and a surface-dwelling (Euproctus asper) salamander. Journal of Experimental Biology 204: 269- 281. https://jeb.biologists.org/content/204/2/269

46 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

Hobbs HH HI, Hobbs HH Jr (1976) On the troglobitic shrimps of the Yucatan Peninsula, Mexico (Decapoda: Atyidae and Palaemonidae). Smithsonian Contributions to Zoology 240: 1-23. https://doi.org/10.5479/si.008 10282.240

Hobbs HH IN, Hobbs HH Jr, Daniel MA (1977) A review of the troglobic decapod crusta- ceans of the Americas. Smithsonian Contributions to Zoology Number 244, Washington, 196 pp. https://doi.org/10.5479/si.00810282.244

Hobbs HH UI (1979) Additional notes on cave shrimps (Crustacea: Atydae and Palaemonidae) from the Yucatan Peninsula, Mexico. Proceedings of the Biological Society of Washington 92(3): 618-633.

Holsinger JR (1977) A new genus and two new species of subterranean amphipod crustaceans (Gammaridae s. lat.) from the Yucatan Peninsula in Mexico. Association for Mexican Cave Studies, Bulletin 6: 15-25.

Holsinger JR (1990) Tuluweckelia cernua, a new genus and species of stygobiont amphipod crustacean (Hadziidae) from anchialine caves on the Yucatan Peninsula in Mexico. Beau- fortia 41: 97-107.

Holthuis LB (1977) Cave shrimps (Crustacea: Decapoda, Natantia) from Mexico. Accademia Nazionale dei Lincei Quaderno 171: 173-195.

Horwitz P, Knott B, Williams WD (1995) A preliminary key to the malacostracan families (Crustacea) found in Australian inland waters. Research Centre for Freshwater Ecology Identification Guide No. 4.Albury, 38 pp.

Hunter RL, Webb MS, Iliffe TM, Bremer JRA (2007): Phylogeny and historical bioge- ography of the cave-adapted shrimp genus Typhlatya (Atydae) in the Caribbean Sea and western Atlantic. Journal of Biogeography. https://doi.org/10.1111/j.1365- 2699.2007.01767.x

Iliffe TM (1992) An annotated list of the troglobitic, anchialine and freshwater cave fauna of Quintana Roo. In: Navarro D, Sudrez-Morales E (Eds) Diversidad Bioldgica en la Reserva de la Biosfera de Sian Ka’an, Quintana Roo, Mexico, Vol. I]. CIQRO, Chetumal, Mexico, 197-215. — https://www.academia.edu/5416051/An_annotated_list_of_the_troglobitic_ anchialine_and_freshwater_fauna_of_Quintana_Roo

Iliffe TM (1993) Fauna troglobia acuatica de la Peninsula de Yucatan. pp. 673-686 in: Biodi- versidad marina y costera de Mexico. S.I. Salazar-Vallejo & N.E. Gonzalez (eds.) Comision National para el Conocimiento y Uso de la Biodiversidad y CIQRO, México, 865 pp.

Iliffe TM, Botosaneanu L (2006) The remarkable diversity of subterranean Cirolanidae (Crustacea: Isopoda) in the peri-Caribbean and Mexican realm. Bulletin de l'Institut Royal des Sciences Naturelles de Belgique. Biologie 76: 5—26. https://dare.uva.nl/ search?identifier=5 1551d10-097d-4609-832f-74bde6066add

Kallmeyer DE, Carpenter JH (1996) Stygiomysis cokei, new species, a troglobitic mysid from Quintana Roo, Mexico (Mysidacea: Stygiomysidae). Journal of Crustacean Biology 16: 418-427. https://doi.org/10.2307/1548897

Lowry JK, Myers AA (2013) A phylogeny and classification of the Senticaudata subord. nov. (Crustacea: Amphipoda). Zootaxa 3610(1): 1-80. https://doi.org/10.11646/ zootaxa.3610.1.1

New distribution records of subterranean crustaceans from cenotes in Yucatan 47

Mejia-Ortiz LM, Hartnoll RG, Lopez-Mejia M (2006) Progressive troglomorphism of ambula- tory and sensory appendages in three Mexican cave decapods. Journal of Natural History 40(5-6): 255-264. https://doi.org/10.1080/00222930600628382

Mejia-Ortiz LM, Lépez-Mejia M, Pakes J, Hartnoll G, Zarza-Gonzalez E (2013) Morphologi- cal adaptations to anchialine environments in species of five shrimp families (Barbouria yanezi, Agostocris bozanici, Procaris mexicana, Calliasmata nohochi and Typhlatya pearsei). Crustaceana 86(5): 578-593. https://doi.org/10.1163/15685403-00003197

Mercado-Salas NE, Morales-Vela B, Sudrez-Morales E, Iliffe T (2013) Conservation status of the inland aquatic crustaceans in the Yucatan Peninsula, Mexico: shortcomings of a pro- tection strategy. Aquatic conservation: Marine and freshwater ecosystems. Wiley Online Library. https://doi.org/10.1002/aqc.2350

Meland K, Mees J, Porter M, Wittmann KJ (2015) Taxonomic Review of the orders My- sida and Stygiomysida (Crustacea, Peracarida). PLoS ONE 10(4): e0124656. https://doi. org/10.1371/journal.pone.0124656

Nicholas G (1962) Checklist of troglobitic organisms of Middle America. American Midland Naturalist 68(1): 165-188. https://doi.org/10.2307/2422643

Olesen J, Boesgaard T, Iliffe TM (2015) The unique dorsal Brood pouch of Thermosbaenacea (Crustacea, Malacostraca) and description of an advanced developmental stage of Tulu- mella unidens from the Yucatan Peninsula (Mexico), with a discussion of mouth part ho- mologies to other Malacostraca. PLoS ONE 10(4): e0122463. https://doi.org/10.1371/ journal. pone.0122463

Ortiz M, Chazaro-Olvera S (2015) A new species of cirolanoid isopod (Peracarida, Isopoda) collected from cenote Aerolito, Cozumel Island, Northwestern Caribbean. Crustaceana 88(2): 152-163. https://doi.org/10.1163/15685403-00003402

Pakes MJ, Weis AK, Mejia-Ortiz L (2014) Arthropods host intracellular chemosynthetic sym- bionts, too: cave study reveals an unusual form of symbiosis. Journal of Crustacean Biology 34(3): 334-341. https://doi.org/10.1163/1937240X-00002238

Pérez-Aranda L (1983a) Atyidae: Typhlatya pearsei. Fauna de los cenotes de Yucatan 3. Univer- sidad de Yucatan, Mérida, 11 pp.

Pérez-Aranda L (1983b) Palaemonidae: Creaseria morleyi. Fauna de los cenotes de Yucatan 1. Universidad de Yucatan, Mérida, 11 pp.

Pérez-Aranda L (1984a) Atyidae: Zyphlatya mitchelli. Fauna de los cenotes de Yucatan 5. Uni- versidad de Yucatan, Mérida, 14 pp.

Pérez-Aranda L (1984b) Cirolanidae: Cirolana anops. Fauna de los cenotes de Yucatan 7. Uni- versidad de Yucatan, Mérida, 13 pp.

Pesce GL, Iliffe TM (2002) New records of cave-dwelling mysids from the Bahamas and Mex- ico with description of Palaumysis bahamensis n. sp. (Crustacea: Mysidacea). Journal of Natural History 36(3): 265-278. https://doi.org/10.1080/00222930010005033

Pohlman JW, Cifuentes LA, Iliffe TM (2000) Food web dynamics and biogeochemistry of anchialine caves: a stable isotope approach. In: Wilkens H, Culver DC, Humphreys WF (Eds) Ecosystems of the World. 30. Subterranean Ecosystems.: Elsevier Science, Amster- dam, 345-357.

48 Dorottya Angyal et al. / ZooKeys 911: 21-49 (2020)

Reddell JR (1977) A preliminary survey of the caves of the Yucatan Peninsula. In: Reddell JR (Ed.) Survey of the caves and cave fauna of the Yucatan Peninsula. Association for Mexican Cave Studies, Bulletin 6: 215-296.

Reddell JR (1981) A review of the cavernicole fauna of Mexico, Guatemala, and Belize. Texas Memorial Museum, The University of Texas at Austin, Bulletin 27, 327 pp. https://www. mexicancaves.org/other/TMM_B27.pdf

Rocha CEF, Iliffe TM, Reid JW, Sudrez-Morales E (1998) A new species of Halicyclops (Co- pepoda, Cyclopoida, Cyclopidae) from cenotes of the Yucatan Peninsula, Mexico, with an identification key for the species of the genus from the Caribbean region and adjacent areas. Sarsia 83: 387-399. https://doi.org/10.1080/00364827.1998.10413698

Rocha CEF, Iliffe TM, Reid JW, Sudrez-Morales E (2000) Prehendocyclops, a new genus of the subfamily Halicyclopinae (Copepoda, Cyclopoida, Cyclopidae) from cenotes of the Yucatan Peninsula, Mexico. Sarsia 85: 119-140. https://doi.org/10.1080/00364827.200 0.10414562

Rocha-Ramirez A, Alvarez EF, Alcocer J, Chavez-Lopez R, Escobar-Briones E (2009) Annotated list of the aquatic epicontinental isopods of Mexico (Crustacea: Isopoda). Revista Mexicana de Biodiversidad 80: 615-631. https://doi.org/10.22201/ib.20078706e.2009.003.159

Ruiz-Cancino G, Mejia-Ortiz LM, Lozano-Alvarez E (2013) Dindmica poblacional de Crea- seriella anops (Crustacea: Isopoda) en cenotes dulceacuicolas de Quintana Roo. In: Lépez- Mejia M, Mejia-Ortiz LM (Eds) La carcinologia en México: El legado del Dr. Alejandro Villalobos 30 afos después. Universidad de Quintana Roo, México DF, 180 pp.

Sanchez-Rodriguez G (2008) Distribucién de la abundancia del ishpodo Creaseriella anops (Creaser, 1936) en sistemas anquihalinos de Quintana Roo, México. BSc Tesis, Universi- dad Nacional Auténoma de México, Facultad de Ciencia, 68 pp.

Schmitter-Soto JJ, Comin FA, Escobar-Briones E, Herrera-Silveira J, Alcocer J, Suarez-Morales E, Elfas-Gutiérrez M, Diaz-Arce V, Marin LE, Steinich (2002) Hydrogeochemical and bio- logical characteristics of cenotes in the Yucatan Peninsula (SE Mexico). Hydrobiologia 467: 215-228. https://doi.org/10.1007/978-94-010-0415-2_19

SEMARNAT (2010) Norma Oficial Mexicana Nom-059-Semarnat-2010, Proteccién ambi- ental- Especies nativas de Mexico de flora y fauna silvestres- Categorias de riesgo y espe- cificaciones para su inclusion, exclusién o cambio- Lista de especies en riesgo. Diario Of- cial, 30 de diciembre de 2010. https://www.dof.gob.mx/normasOficiales/4254/semarnat/ semarnat.htm

Sudrez-Morales E, Rivera Arriaga E (1998) Hidrologia y fauna acuatica de los cenotes de la Peninsula de Yucatan. Revista de la Sociedad Mexicana de Historia Natural 48: 37—47. http://bibliotecasibe.ecosur.mx/sibe/book/000054250

Sudrez-Morales E, Ferrari FD, Iliffe TM (2006) A new epacteriscid copepod (Calanoida: Epacteriscidae) from the Yucatan Peninsula, Mexico, with comments on the biogeogra- phy of the family. Proceedings of the Biological Society of Washington 119(2): 222-238. https://doi.org/10.2988/0006-324X(2006) 119[222:ANECCE]2.0.CO;2

Tinnizi NM, Quddusi BK (1993) An illustrated key to Malacostraca (Crustacea) of the North- ern Arabian Sea. Pakistan Journal of Marine Sciences 2(1): 49-66. https://aquaticcom- mons.org/16058/1/PJMS2.1_049.pdf

New distribution records of subterranean crustaceans from cenotes in Yucatan 49

Wagner HP (1994) A monographic review of the Thermosbaenacea (Crustacea: Peracarida). A study on their morphology, taxonomy, phylogeny and biogeography. Zoologische Verhan- delingen 291(3): 1-338. https://www.jstor.org/stable/20088754

Webb MS (2003) Intraspecific relationships among the stygobitic shrimp Typhlatya mitchelli, by analyzing sequence data from mitochondrial DNA. MSc Thesis, Texas, United States of America: Texas A&M University. http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1 .1.174.684&rep=rep 1 &type=pdf

Yager J, Madden ME (2010) Preliminary analysis of the ecology of a cenote in Quintana Roo, Mexico, characterized by its extraordinary quantities of remipedes. Karst Frontiers, Karst

Water Institute Special Publication 7: 138-140.