Bahadzia yagerae Ortiz and Peréz, 1995

Bahadzia yagerae Ortiz and Peréz, 1995 View in CoL

( figures 6–8 View FIG View FIG View FIG )

Bahadzia yagerae Ortiz and Peréz, 1995: 166–168 , figures 1–4 View FIG View FIG View FIG View FIG [type-locality: Cueva Susana, Playa Girón, Metanzas Province, Cuba].

Material examined. Cuba. Metanzas Province : Cueva Susana, Playa Girón, five paratypes, J. Yager, 27 June 1994, and two paratypes, D. Williams, 11 September 1992 .

Holotype (not examined in the present study) deposited in the collection of the Institute of Ecology and Systematics of the Department of Science, Technology and Environment, Cuba. The paratypes are in the collection of J. R. Holsinger ( H-3250 , H-3792 ) .

Diagnosis. Small to medium-sized stygobitic species, similar to Bahadzia caymanensis and B. patilarga by having a tiny, round, pigmentless eye, but differing from all other species of Bahadzia by possession of at least 50 pectinate spines on distal end of outer plate of maxilla 1.

Female. Corresponding to the description of Ortiz and Peréz (1995) with the following additions and corrections. Mandible: molar well developed; spine row with about 11 weakly serrate spines; lacinia mobilis of left mandible fourdentate, that of right two-dentate and smaller; incisor of left mandible fivedentate, that of right five-dentate and narrower; palp segment 3 subequal to the combined lengths of 1 and 2, bearing long row of approximately 22–23 D setae and three to four E setae; A, B and C setae absent. Lower lip: inner lobes present and distinct; lateral processes short, rounded apically. Maxilla 1: inner plate with 17 short, lightly plumose setae: outer plate bearing at least 50 pectinate spines; left and right palps similar, expanded and rounded distally, broad apex with nine blade spines and one short, naked seta. Maxilla 2: inner plate narrowing distally, with row of approximately 48 naked submarginal facial seatae and row of approximately 17 thicker setae located on extreme inner margin. Maxilliped: apices of inner plate even, armed on entire distal end with approximately nine short spines, inner margin with row of 17 weakly plumose setae; outer plate rounded distally, armed with single short spine on distal margin and few naked setae; palp segment 3 pubescent distally, distal inner margin of segment 3 not lobate; palp segment 4 as long as segment 3, nail small and spine-like. Gnathopod 1: propod subrectangular, about twice as long as broad, posterior margin heavily setose distally, palm short, transverse but lobate at defining angle and bearing three spines on lobe; carpus approximately 80% longer than propod, bearing several clusters of long setae on posterior margin and toward distal end; merus weakly lobiform and pubescent; basis with 12 long setae; coxa long and deep with about three to four short spines and eight to nine short setae. Gnathopod 2: propod subrectangular, palm short, oblique, bearing three long setae at defining angle, posterior margin with six sets of long setae, anterior margin with three sets of setae; carpus approximately 20% longer than propod, posterior margin with nine clusters of long setae; basis with six long setae on posterior margin; coxa deeper than broad, margin with 12 short setae.

Pleopods normal, peduncles each with two rather large coupling spines, and one unmodified spine on distal inner margin. Uropod 1: inner ramus shorter than peduncle, longer than outer ramus bearing about five spines; peduncle with 13 spines, one of which is basofacial in position. Uropod 2: inner ramus subequal in length to peduncle, longer and broader than outer ramus, armed with 11 spines; outer ramus with about six spines; peduncle with 12 spines, eight of which form a comb row on dorsodistal end. Uropod 3: approximately 15% length of the body; inner ramus slightly larger than outer ramus, margins with short spines and plumose setae; outer ramus with short terminal segment, inner margin with short spines and plumose setae, outer margin with spines only; peduncle with six spines. Telson rather long and narrow, in two separate lobes; lateral margins with about six spines, none in sets of two; medial margins with two to four spines, apices each with one or two small spines and three long, distally plumose setae.

Male. Differing from female in structure of gnathopod 2 as follows: dactyl and propod proportionately longer; propod palm long, oblique with double row of about 14 blunt-tipped spines, defining angle with three long setae, posterior margin longer than palm with four sets of setae.

Distributional ecology. This species is known only from its type-locality, Cueva Susana, an anchialine cave on the southern coast of Cuba. Specimens were collected at or below the halocline from a depth of approximately 15 m in water with 35 ppt salinity.

Remarks. In the original description by Ortiz and Pérez (1995), the holotype was said to be 1.5 cm in length, but this was an error inasmuch as both the drawing and description indicated the holotype to be only 5 mm (0.5 cm) in length. This error was inadvertently repeated by Jaume and Wagner (1998).

Phylogenetic analysis

Cladistic methods. A phylogenetic analysis was performed using PAUP, version 4.0b10, in which all characters were left unordered and unweighted. During all searches the ancestral condition was left ‘unknown’. Character states were not assigned relative to a primitive/derived condition, i.e. a character state of 0 does not necessarily reflect the primitive state. During the Bootstrap analysis, the following options were in effect: full heuristic search with 1000 bootstrap replicates, and 50% majority rule consensus; tree bisection and reconnection (TBR) branch swapping was performed on minimal trees only (steepest descent by random stepwise addition), Multrees option in effect. The resulting tree was evaluated and edited in MacClade Version 4.0.

Taxa. The cladistic analysis was perfomed on the genus Bahadzia , and eight other outgroup genera within the Hadziidae / Melitidae family complex ( table 1 View Table 1 ). The choice of outgroups used was based on a number of different criteria. Protohadzia and Saliweckelia are fully marine genera within the family Hadziidae , living in shallow coastal waters in the Caribbean. Metaniphargus is found in the freshwater layer of an anchialine cave in Venezuela and in brackish water in anchialine caves throughout the greater Caribbean and in the intertidal zone from Oahu, Hawaii. These genera are potentially related to Bahadzia . Holsinger (1992) conducted a cladistic analysis on the genus Bahadzia and 13 genera of the ‘weckeliid group’ in the family Hadziidae . This analysis suggested that two of the ‘weckeliid group’ genera, Mayweckelia and Tuluweckelia , are sister genera to Bahadzia and may even be derived from a Bahadzia -like ancestor. Mayaweckelia and Tuluweckelia were included in the present analysis to explore further this relationship using a different and larger data set. Melita stocki Karaman was included as a very generalized hadziid/melitid type.

With the exception of Melita stocki , Protohadzia schoenerae Zimmerman and Barnard , and the two species of Saliweckelia , whose character states were based on descriptions and drawings from the literature, all other species used in this analysis were examined from preserved material (see Appendix for a list of the characters).

Results

The phylogeny shown in figure 9 View FIG suggests that the genus Bahadzia may not be monophyletic, inasmuch as B. latipalpus Stock and B. jaraguensis Jaume and Wagner are in the same clade as the sister genera Mayaweckelia and Tuluweckelia . All other Bahadzia species are found within one clade, which in turn is divided into two groups: those species found in the Bahamas and Turks and Caicos Islands, and those found in Cuba, Mexico and the Cayman Islands. The Bahamas / Turks and Caicos clade is relatively well defined. Bahadzia williamsi Holsinger and B. stocki Holsinger form one pair of sister species, and B. setimana Stock and B. oblique Stock form another pair. The two Yucatan species, B. bozanici Holsinger and B. setodactylus Holsinger , do not form sister species and the two Cuban species, B. yagerae and B. patilarga , also do not fall out as sister species in the analysis. However, these four species and B. caymanensis collectively form a western Caribbean clade. The two species found on the island of Hispaniola, B. latipalpus and B. jaraguensis , are sister species in this analysis and form a clade with the outgroup genera Mayaweckelia and Tuluweckelia .

Discussion

Based on the geographic distribution of Bahadzia , most species of which are clustered in widespread insular habitats ( figure 10 View FIG ), it could be hypothesized that the derived phylogeny would be highly predictable and resolved. The presently known species of Bahadzia are restricted to the Bahamas, Cuba, Hispaniola, Yucatan Peninsula (including Cozumel Island) and the Cayman Islands. With two exceptions, there appears to be a relationship between species distribution and phylogeny. The species found in the Bahamas / Turks and Caicos group together and the Hispaniola species group together. However, the species found in Cuba and the Yucatan Peninsula of Mexico do not form nested subgroups relative to their geographic distribution. Given the close geographic proximity of these species, this lack of resolution is surprising. For instance, the type-localities of the two Cuban species, B. patilarga and B. yagarae , are separated by only 17 km. Although B. latipalpus and B. jaraguensis do form a nested subgroup relative to their distribution, they also form a clade with the outgroup genera Mayaweckelia and Tuluweckelia .

Most species of Bahadzia live within a very narrowly defined ecological niche at or near the halocline in anchialine caves. Physiochemical in situ measurements in these caves, such as Mayan Blue Cenote, a cave on the Yucatan Peninsula where B. bozanici is found, have shown a large drop in oxygen levels at the halocline to less than 1 mg /l ( Pohlman et al., 1997). Most species of Bahadzia have very large coxal gills relative to other stygobitic and epigean amphipod species, and this may be an adaptation to living and feeding within this low oxygen environment. Pohlman et al. (1997) conducted a stable isotope study of the water in Mayan Blue Cenote and concluded that chemoautotrophic nitrifying bacteria played a key role as the base of the food chain for the stygobitic fauna in this cave. In anchialine caves of Cuba inhabited by Bahadzia, Yager (1994) reported measurements of dissolved oxygen, temperature and salinity similar to those in Mayan Blue Cenote. Most species of Bahadzia appear to be adapted to life in this unique ecosystem typical of anchialine cave waters. The base of the food chain may be a chemoautotrophic bacterium located at the halocline of these caves, where temperature, salinity and oxygen requirements appear to be very narrowly defined. Bahadzia is not the only crustacean that is adapted to this specific physical and chemical environment. A number of other taxa of crustaceans are almost always found living sympatrically with Bahadzia , including thermosbaenaceans, remipedes, cirolanid isopods and ostracods. Pohlman et al. (1997) were able to define the trophic structure of these crustacean groups within Mayan Blue Cenote. Based on the data reported by these workers, we suggest that there are very specific physical, chemical and biological selective pressures acting on species of Bahadzia and other crustaceans living at or near the halocline in anchialine caves. Moreover, these selection pressures are apparently very different from those found in most other aquatic subterranean habitats.

With regard to habitat, Bahadzia latipalpus and B. jaraguensis are exceptional in comparison with the eight species recorded from anchialine waters; however, as previously noted the ecology of B. caymanensis is unclear. Bahadzia latipalpus was collected from fresh and oligohaline well water ( Stock, 1985) and B. jaraguensis was taken from weakly brackish water on the cave floor in mats of filamentous green algae ( Jaume and Wagner, 1998). It is perhaps significant that Mayaweckelia and Tuluweckelia also occur in either fresh or weakly brackish water ( Holsinger, 1977, 1990) and that an earlier cladistic analysis by Holsinger (1992) of ‘weckeliid group’ genera and the genus Bahadzia suggested that Mayaweckelia and Tuluweckelia are sister genera to Bahadzia . Our present analysis offers further support of this hypothesis. In contrast to the anchialine cave-dwelling species of Bahadzia , B. latipalpus and B. jaraguensis live under very different physiochemical and biological selection pressures and display morphological differences as well. Holsinger (1992) suggested that the putative common ancestor of Bahadzia , Mayaweckelia and Tuluweckelia might not have differed significantly from modern Bahadzia . With the exception of two characters, which include absence of the mandibular palp and second segment of the outer ramus of uropod 3, both apparently relatively uncomplicated structural losses, Mayaweckelia and Tuluweckelia share more apomorphic characters with Bahadzia than any ‘weckeliid group’ genus. Moreover, both Mayaweckelia and Tuluweckelia were excluded from the ‘weckeliid group’ in a recent redefinition of the group by Holsinger and Ruffo (2002).

Our observations suggest that strong selection pressures may act on marine amphipods that invade anchialine and later freshwater caves, and that these pressures may result in morphological convergence of species from different lineages. Conceivably, this has occurred in the species of Bahadzia on Hispaniola and the species of Mayaweckelia and Tuluweckelia on the Yucatan Peninsula. Continued research utilizing molecular data may assist in resolving the phylogeny of Bahadzia and determine whether or not this genus is monophyletic. Molecular data may also help us to clarify the relationship between Bahadzia and other species in the hadziid/melitiid family complex.