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Description of Two New Species of the Midas Cichlid Complex (Teleostei: Cichlidae) from Lake Apoyo, Nicaragua

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Description of Two New Species of the Midas Cichlid Complex (Teleostei: Cichlidae) from Lake Apoyo, Nicaragua PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON 123(2):159–173. 2010. Description of two new species of the Midas cichlid complex (Teleostei: Cichlidae) from Lake Apoyo, Nicaragua Matthias F. Geiger, Jeffrey K. McCrary, and Jay R. Stauffer, Jr.* (MFG) Bavarian State Collection of Zoology (ZSM), Department of Ichthyology, Mu¨nchhausenstr. 21, 81247 Munich, Germany; (JKM) Fundacio´n Nicaragu¨ense Pro-desarrollo Comunitario Integral (FUNDECI/GAIA), Estacio´n Biolo´gica, Laguna de Apoyo Nature Reserve, Nicaragua; (JRS) School of Forest Resources, 432 Forest Resources Building, The Pennsylvania State University, University Park, Pennsylvania 16802, U.S.A., e-mail: [email protected] Abstract.—Two species belonging to the Amphilophus citrinellus (Gu¨nther, 1864) species complex endemic to Lake Apoyo, Nicaragua are described. Both species exhibit unique phenotypic characters that have not been found in other members of the species complex. Furthermore, they breed assortatively in Lake Apoyo and can readily be distinguished in the field from all other described species found in that lake. Including the two herein described species, six species that form a monophyletic species assemblage within the Midas cichlid complex inhabit Lake Apoyo, Nicaragua. Midas cichlids are monogamous sub- allowed the description of three endemic strate spawners that form pairs only species from Lake Xiloa´ in 2002 and three during breeding season, when they ag- endemic species from Lake Apoyo in gressively defend their territory and fry. 2008 (Stauffer & McKaye 2002, Stauffer The name Midas cichlid derives from the et al. 2008). Findings from molecular fact that, in some Nicaraguan lakes, genetic studies suggested that both Lake brightly coloured Amphilophus individu- Xiloa´ and Lake Apoyo contained other als can be found that have lost the undescribed Amphilophus and that all melanophores that build patterns of black examined individuals in one lake are bars, yielding individuals ranging in color closely related to each other based on from white to orange or red, and collec- microsatellite genotyping of three loci tively termed ‘gold.’ They are found in (McKaye et al. 2002). This conclusion varying abundance in more turbid lakes was supported by mitochondrial DNA but not in Lake Apoyo (Barlow 1976). sequence data, which demonstrated that The Midas cichlid complex makes an fishes from Lake Apoyo were more excellent study subject for evolutionary closely related to each other than to fishes biology and taxonomy. Historically, Bar- from other lakes (Barluenga & Meyer low & Munsey (1976) recognized only 2004, Barluenga et al. 2006). three species in the Midas cichlid com- The recent origins of Lakes Xiloa´ plex; however, we are now able to (,10,000 bp, BANIC 1977) and Apoyo differentiate several species. Field obser- (,23,000 bp; BANIC 1977, Sussman vations using SCUBA, extensive collect- 1985) coupled with their endemic Midas ing efforts, and proper treatment of cichlids has inspired biologists to specu- collected material for museum collections late and investigate the possibility of sympatric speciation (Barlow 1976, Mc- * Corresponding author. Kaye et al. 2002, Barluenga et al. 2006, 160 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON but see Schliewen et al. 2006). The small Amphilophus. Gobiomorus dormitor and at size of Lake Apoyo (20.92 km2 surface least three species of tilapias have been area) and its rather homogeneous habitat introduced in the past two decades (Waid with syntopic breeding of its endemic et al. 1999, McCrary et al. 2007). There Amphilophus species (McCrary & Lo´pez are no open-water connections to any 2008), support the theory that sympatric other water body; thus, it is speculated speciation has occurred (Wilson et al. that these fishes might have entered the 2000, Barluenga et al. 2006). lake via humans, piscivorous birds, and/ A complete taxonomic inventory of the or climatic events (Stauffer et al. 2008). region is essential to discover the biologi- cally most meaningful explanations of the Materials and Methods phylogenetic history within the Midas cichlid complex. We provide here a descrip- We collected fishes in three field trips tion of the fifth and sixth members of Lake during the dry seasons (Nov–Apr) of 2006/ Apoyo’s endemic species of Amphilophus. 2007, 2007/2008, and 2008/2009. Individ- uals were caught by SCUBA divers using harpoons following field identification. Site Description Fishes were anesthetised, preserved in Lake Apoyo is situated within an 10% formalin, individually tagged, and almost circular volcanic caldera of fin-samples taken for molecular genetic 36.32 km2, about 4 km west of Lake studies. Photos of live individuals were Nicaragua. The lake’s water surface takenandnotesoncolorationmadeinthe occupies 20.92 km2; its diameter measur- field. Fins were pinned, fishes preserved in ing more than 4 km with a maximum 10% formalin, and permanently preserved depth 178 m (CIRA 2008). The caldera in 70% ethanol. Counts and measurements was created by a series of volcanic follow Barel et al. (1977) and Stauffer eruptions, the last one occurred about (1991, 1994), except that head depth was 23,000 years ago (Sussman 1985). The measured from the hyoid symphysis to the water level of Lake Apoyo is 70 m above top of the head at 90u angle to the sea level (masl), with effluents limited to horizontal body axis. Measurements are subterranean filtration through highly point-to-point using a dial calliper to the permeable geologic layers toward neigh- nearest 0.01 mm, and taken from the left boring Lake Nicaragua (31 masl; side of specimens. Following abbreviations 5.4 hm3 pa). The lake has undergone a are used in the tables: 15 m decrease in water level since 1950 ADAA—anterior insertion of dorsal fin to (CIRA 2008). The water of oligotrophic anterior insertion of anal fin; Lake Apoyo is warm (27–29.5uC), alka- PDPA—posterior insertion of dorsal fin to line (pH 5 8.1), and rather saline with a posterior insertion of anal fin; conductivity of 3310 mS and Na+ of ADPA—anterior insertion of dorsal fin to 640 mg/l (Parello et al. 2008). posterior insertion of anal fin; Compared to some of the smaller PDAA—posterior insertion of dorsal fin to volcanic crater lakes in Nicaragua, the anterior insertion of anal fin; PDVC—posterior insertion of dorsal fin to fish fauna of Lake Apoyo is depauperate ventral portion of caudal fin; (Waid et al. 1999) and the native forms PADC—posterior insertion of anal fin to include: one atherinid Atherinella sardina, dorsal portion of caudal fin; one poeciliid Poecilia cf. sphenops,and ADPV—anterior insertion of dorsal fin to several cichlids: Parachromis managuensis insertion of pelvic fin; and at least six (four of which have been PDPV—posterior insertion of dorsal fin to described) endemic species of the genus insertion of pelvic fin. VOLUME 123, NUMBER 2 161 Additionally, we examined the caudal Amphilophus native to Lake Apoyo. To skeletons of ten individuals of each of the that purpose, we obtained meristic and six Lake Apoyo species of Amphilophus morphometric data for the holotypes and using high-resolution x-ray pictures. We seven paratypes each of, A. astorquii, A. only used specimens with complete and chancho,andA. flaveolus as well as eight straight caudal-fin rays and counted the paratypes of A. zaliosus (see comparison number of: principal (segmented) rays, material). dorsal and ventral procurrent rays (sensu Chakrabarty 2007), procurrent and prin- Results cipal rays inserting at the haemal spine of the preural centrum (sensu De Schepper Amphilophus supercilius, new species et al. 2004), principal rays of the parhy- Fig. 1, Table 1 pural (sensu Chakrabarty 2007), and Holotype.—ZSM 38821, adult male, principal rays inserting in each hypural. 166.6 mm SL, 27 Feb 2007, Spanish We also measured the length of the first Coast, Lake Apoyo NE shore, Nicara- ventral principal caudal-fin ray and the gua, 11u5695.430N, 86u00946.880W, DNA length of the lower central caudal-fin ray. tag: 247. Since sex of Midas cichlids can only be Paratypes.—All paratypes were collect- determined by invasive methods or direct ed from Lake Apoyo, Nicaragua. ZSM observation of breeding pairs, we did not 37347, 163.6 mm SL, 11 Feb 2008, rock group individuals according to sex and formation called ‘‘los hongos,’’ S shore, did not test for sexual dimorphism in 11u54920.790N, 86u01945.400W, DNA tag: morphometrics. Institutional abbrevia- 735. ZSM 37348, 142.4 mm SL, 11 Feb tions follow Leviton et al. (1985). Mor- 2008, rock formation called ‘‘los hongos,’’ phometric data were analyzed using S shore, 11u54920.790N, 86u01945.400W, sheared principal component analysis DNA tag: 723. ZSM 37351, 2, 157.8– (SPCA), which factors the covariance 166.7 mm SL, 11 Feb 2008, rock forma- matrix and restricts size variation to the tion called ‘‘los hongos,’’ S shore, first principal component (Humphries et 11u54920.790N, 86u01945.400W, DNAtags: al. 1981, Bookstein et al. 1985). Meristic 728 & 736. ZSM 38751, 143.2–146.3 data were analyzed using principal com- mm SL, 22 Jan 2007, Fte Ranchos, ponent analysis (PCA) in which the 11u55954.000N, 86u03910.800W, DNAtags: correlation matrix was factored. Compar- 50 & 164. ZSM 38752, 159.9 mm SL, isons among species were illustrated by 17 Apr 2009, Fte Cruz de Mayo, plotting the sheared second and third 11u55929.140N, 86u03922.040W, DNA tag: principal components (2SPCA, 3SPCA) 629. ZSM 38753, 3, 129.8–148.9 mm SL, of the morphometric data or the 2SPCA 19 Jan 2007, Fte Ranchos, 11u55954.000N, and first principal components (PCA) of 86u03910.800W, DNA tags: 39, 42, & 59. the meristic data. The Statistical Analysis ZSM 38754, 150.8 mm SL, same data as System (SAS) software was used to for holotype, DNA tag: 250. PSU 4768, calculate both PCA and SPCA. 132.5–167.8 mm SL, same data as for As the monophyly of Lake Apoyo’s holotype, DNA tags: 251 & 252.
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