Untangling Confusion between vernalis and Eubranchipus neglectus (: ) Author(s): Denton Belk, Graziella Mura, Stephen C. Weeks Source: Journal of Biology, Vol. 18, No. 1 (Feb., 1998), pp. 147-152 Published by: The Crustacean Society Stable URL: http://www.jstor.org/stable/1549529 Accessed: 11/11/2010 16:16

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http://www.jstor.org JOURNALOF CRUSTACEANBIOLOGY, 18(1): 147-152, 1998

UNTANGLING CONFUSION BETWEEN EUBRANCHIPUS VERNALISAND EUBRANCHIPUSNEGLECTUS (BRANCHIOPODA: ANOSTRACA)

Denton Belk, Graziella Mura, and Stephen C. Weeks

ABSTRACT Despiteillustrations in Garman(1926) clearlyshowing the differentantennal appendages of Eu- branchipus vernalis and Eubranchipus neglectus, Creaser (1930) published erroneous drawings of the antennalappendages of these two species thatled to more than65 years of taxonomicconfu- sion betweenthem. We untanglethis confusion,and show thatthese species have nonoverlapping areasof occurrencewith E. vernalisto the eastand E. neglectusto the westof the AppalachianMoun- tains.In addition,we presentevidence supporting the use of resting-egg(cyst) morphologyin study- ing evolutionaryrelationships among anostracan species. An importantpart of this usefulnessis due to the independenceof cyst morphologyfrom sexual selection.Since the primarytaxonomic char- actersof anostracansare all stronglyinfluenced by sexualselection, cyst morphologycan supplya reasonablyindependent set of charactersfor testinghypotheses of speciesrelationships.

Nine of the 16 anostracanspecies described similarity,a situation that usually indicates in the genus Eubranchipusare endemic to close relationship. North America (Belk and Brtek, 1995). Of Brendonck et al. (1992) found that four these nine, two species pairs, bundyi-intrica- Africanspecies in the anostracangenus Strep- tus and holmanii-moorei,were involved in tocephalusproduce uniquely shaped tetrahe- taxonomic problemsthat have alreadybeen dral cysts. Their morphologicalanalysis of cleared up. Here we reveal and correctcon- the taxonomicallyimportant male antennae fusioninvolving a thirdspecies pair, vernalis- suggestedthese four streptocephalidsform a neglectus.In addition,we show thatthe mor- closely relatedgroup. Thus, as it turnedout, phology of the cyst shell reflects the appar- the unique tetrahedralcyst representedthe ent close evolutionaryrelationship between most striking of a cluster of morphological the sister species of each pair. charactersindicating close evolutionaryre- Hartland-Rowe(1967) pointedout thattwo lationship.Brendonck et al. formallyrecog- taxawere being confusedunder the nameEu- nized this situationby assigningthe four spe- branchipus bundyi Forbes, 1876. He docu- cies to a new subgenus, Parastreptocephalus. mented the morphologicaldifferences, and This is the first example of cyst morphology described a new species, Eubranchipus intri- aiding in the discovery of a groupof closely catus Hartland-Rowe, 1967. Brtek (1967) relatedanostracans. demonstratedthat the taxon from southern As was the case in the groupof relatedspe- Louisianareferred to in severalstudies by Dr. cies which Brendoncket al. (1992) named Walter G. Moore as Eubranchipus holmanii Parastreptocephalus, we found each of the (Ryder,1879) was in fact a new specieswhich threepairs of problemspecies of Eubranchi- he named Eubranchipus moorei Brtek, 1967. pus producecysts that look alike in compar- We point out below that a mistake in fig. 3 isons made between the members of each of Creaser(1930) resulted in confusion be- pair.The threespecies that have not been con- tween (Verrill, 1869) fused with other taxa (Eubranchipus ore- and Eubranchipus neglectus Garman, 1926. gonus Creaser, 1930, Eubranchipus ornatus Creaser'serror was picked up and perpetu- Holmes, 1910, and ated in popular identificationkeys by Pen- Forbes, 1876) producecysts that look differ- nak (1953, and later editions) and by Dexter ent from each other,and from cysts of all the (1959). Brtek(1966) incorrectlyplaced these other North Americanspecies. two in synonymy,while hesitantlysuggesting the neglectus form might be a subspecies. MATERIALSAND METHODS Confusion between the taxa within each of All cystsused in thisstudy were removed from the brood these threepairs resulted from morphological pouchesof preservedspecimens. We chose only cysts that

147 148 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 18, NO. 1, 1998

Figs. 1, 2. Dorsal views of left antennal appendages. 1, Eubranchipus neglectus, antennal appendage from a 25-mm male collected in Cuyahoga County, Ohio, U.S.A. (DB146); 2, Eubranchipus vernalis, antennal appendage from a 20-mm male collected in New London County, Connecticut, U.S.A. (DB1095). Scales = 1 mm. appearedto be mature and of normal morphology, so as to male by SEM. When materialwas available, we used cysts avoid problems like those discussed in Mura (1992). The from several populations, choosing especially those distant selected cysts were preparedfor SEM analysis as described from each other. For our figures, we selected the SEM in Mura (1986). We used cysts of 1-5 females from each photographs that most accurately illustrated the typical location, and examined more than 4 cysts from each fe- morphology of the cyst produced by each species.

Figs. 3, 4. Cysts, whole view (a) and close view of surface (b). 3, Eubranchipus holmanii; 4, Eubranchipus moorei. Scales: a = 100 am; b = 20 ,um. BELK ETAL.: SYSTEMATICS AND CYST MORPHOLOGY OF EUBRANCHIPUS 149

Figs. 5-8. Cysts, whole view (a) and close view of surface (b). 5, Eubranchipus bundyi; 6, Eubranchipus intricatus; 7, Eubranchipus vernalis; and 8, Eubranchipus neglectus. Scales: a = 200 lim; b = 50 jim. 150 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 18, NO. 1, 1998

Figs. 9-11. Cyst, whole view (a) and close view of surface (b). 9, Eubranchipus ornatus; 10, Eubranchipus serra- tus; and 11, Eubranchipus oregonus. Scales: a = 100 gm; 9b = 20 gm; 10b and lb = 50 gm.

We used cysts from the following sources and locali- serratus: DB152 Coconino County, Arizona, U.S.A.; ties during the SEM portion of our study. For E. bundyi: DB581 British Columbia, Canada; and DB663 Beaver- DB222 (DB = collection of Denton Belk) Apache County, head County, Montana, U.S.A. For E. vernalis: DB 1095 Arizona, U.S.A.; DB229 Coconino County, Arizona, New London County, Connecticut, U.S.A. and YPM8247 U.S.A.; DB528 Alberta, Canada; and DB792 Northwest (YPM = Peabody Museum of Natural History, Yale Uni- Territories, Canada. For E. holmanii: DB517 Madison versity) New Haven County, Connecticut, U.S.A. County, Alabama, U.S.A. For E. intricatus: DB554 Al- Data for the map in Fig. 12 came from field work by berta, Canada, and DB557 Alberta, Canada. For E. Stephen Weeks in Ohio during the period 26 July 1995 moorei: DB521 Mobile County, Alabama, U.S.A., and and 1 May 1996, and locality data on collections in the DB524 (paratypes) St. Tammany Parish, Louisiana, holdings of the National Museum of Natural History, U.S.A. For E. neglectus: DB 146 Cuyahoga County, Ohio, Smithsonian Institution; the Milwaukee Public Museum, U.S.A.; DB518 Madison County, Alabama, U.S.A.; Milwaukee, Wisconsin, U.S.A.; the Peabody Museum of DB880 Madison County, Alabama, U.S.A.; and accession Natural History, Yale University; the Canadian Museum no. IZ1994-12 (Milwaukee Public Museum, Milwaukee, of Nature, Ottawa, Ontario; the personal collection of Wisconsin, U.S.A.) Jefferson County, Kentucky, U.S.A. Denton Belk; and specimens examined by Belk for Harp For E. oregonus: DB727 King County, Washington, et al. (in press). These specimens are divided among the U.S.A. For E. ornatus: DB530 Alberta, Canada. For E. Smithsonian Institution, Arkansas State University Mu- BELK ETAL.: SYSTEMATICS AND CYST MORPHOLOGY OF EUBRANCHIPUS 151

vernalis by comparing Figs. 7 and 8. In ad- dition, very similar ridge development, dif- fering only in width, suggested that bundyi, intricatus, neglectus, and vernalis may be a cluster of related species (Figs. 5-8). Each of the three species of Eubranchipus that have not been subjects of taxonomic problems had a unique cyst-shell patternin comparison to all the other North American species (Figs. 9-11). For these three, cyst morphology offered no suggestion of their relationships among the North American Eubranchipus fauna. Our study of the distributions of E. ne- glectus and E. vernalis shows that they have nonoverlapping areas of occurrence sepa- rated by the Appalachian Mountains (Fig. 12). All verified records of E. vernalis were east of the Appalachians, from Connecticut - _ - _ {____, d^ V Apaiacnians south to Columbia, South Carolina. All ver- ified records of E. neglectus were confined Fig. 12. Distribution of Eubranchipus neglectus and Eu- to the area between the western slope of the branchipus vernalis, based on specimens in museum and Appalachian Mountains and the Great Plains private collections (see Materials and Methods for details). from Ontario in Canada south to northern Al- abama in the United States, and as far west seum, and Denton Belk (DB1231, 1232, 1250, 1251). All as Arkansas. museum collections were personally examined by Den- Our of collected ton Belk. study specimens through- out eastern North America reveals that the Appalachian Mountains separate the ranges RESULTS AND DISCUSSION of Eubranchipus neglectus and Eubranchipus Our Figs. 1 and 2 show that Eubranchipus vernalis. Thus, it seems clear that the infor- neglectus and E. vernalis are reliably identi- mation reported in Dexter (1946), Dexter and fied by the differing morphology of their an- Kuehnle (1951), Dexter (1967), and many of tennal appendages. Garman (1926) under- the papers cited in these works, actually ap- stood this, and accurately illustrated the an- plies to E. neglectus, and not to E. vernalis. tennal appendages of both these species We know for certain that this is the situation (compare his figs. C and D to ours). Problems in Modlin (1982, 1983, 1985) and Belk and began when Creaser (1930) misidentified the Milne (1984), because we have examined specimen that he used to draw his fig. 3 to specimens from these studies. Ferguson illustrate the antennal appendage of E. ver- (1935) reported the first Canadian record for nalis. The specimen he used for the drawing what he thought was E. vernalis. Fortunately, was actually one of E. neglectus. Creaser pub- he placed specimens at the Canadian Museum lished his 1930 paper as a revision of the of Nature. These allow us to determine that genus Eubranchipus, giving it standing as au- he was dealing with E. neglectus. thoritative. Thus, not unexpectedly, the widely After presenting new observations and re- used identification keys of Pennak (1953, and viewing the data on anostracan cyst mor- later editions) and Dexter (1959) reproduced phology, Thiery et al. (1995) concluded that Creaser's drawing, and further clouded the cyst morphology can provide new taxonomic separate identity of these two species. information useful in defining natural groups. The grouping of our cyst photographs on We concur. In addition, we point out that the basis of morphological similarity brought characters based on cysts may be particularly together each of the pairs of species that have useful, because they are independent of sex- generated the most taxonomic confusion. This ual selection, unlike the other morphological can be seen for holmanii-moorei by compar- characters used in anostracan (for ing Figs. 3 and 4, for bundyi-intricatus by discussion, see Belk, 1991; Brendonck, comparing Figs. 5 and 6, and for neglectus- 1995). Thus, they likely offer a reasonably in- 152 JOURNALOF CRUSTACEANBIOLOGY, VOL. 18, NO. 1, 1998

dependent set of characters against which hy- . 1967. Annual changes in populations of Anos- potheses of relationship may be tested. traca Crustacea.-Symposium on Crustacea. Marine Biological Association of India, Mandapam Camp, In- dia 2: 568-576. ACKNOWLEDGEMENTS , and C. H. Kuehnle. 1951. Furtherstudies on the For supplying specimens, we thank David B. Donald, fairy shrimp populations of northeastern Ohio.-Ohio Clyde H. Eriksen, George L. Harp, Joan P. Jass, Eric A. Journal of Science 51: 73-86. Lazo-Wasem, Walter D. Milne, Jr., Richard E. Modlin, Ferguson, M. S. 1935. Three species of Eubranchipus Walter G. Moore, Donald J. Pinkava, Judith C. Price, new to Canada.-Canadian Field-Naturalist49: 47-49. Kenneth A. L. Reading, and Stephen Spotte. Stephen C. Garman, H. 1926. A new phyllopod crustacean from Weeks was funded by grants NGSCA-95-01 and FANM Kentucky.-Transactions of the Kentucky Academy of 13 from the Ohio Department of Natural Resources' Di- Science 1: 85-87. vision of Wildlife. Harp, G. L., G. Leeds, and H. W. Robison. (In press.) First report on the fairy shrimps (Branchiopoda: Anos- traca) of Arkansas.-Southwestern Naturalist. LITERATURECITED Hartland-Rowe,R. 1967. Eubranchipus intricatus n. sp., Belk, D. 1991. Anostracan mating behavior: a case of a widely distributedNorth American fairy-shrimp,with scramble-competitionpolygyny.-In: R. T. Bauer and J. a note on its ecology.-Canadian Journal of Zoology W. Martin,eds., Crustaceansexual biology. Pp. 111-125. 45: 663-666. Columbia University Press, New York, New York. Modlin, R. F. 1982. A comparison of two Eubranchi- , and J. Brtek. 1995. Checklist of the Anos- pus species (Crustacea: Anostraca).-American Mid- traca.-Hydrobiologia 298: 315-353. land Naturalist 107: 107-113. , and W. D. Milne, Jr. 1984. Anostraca in Al- . 1983. Effect of temperature and body size on abama.-Journal of the Alabama Academy of Science oxygen consumption of two species of Eubranchipus 55: 245-247. (Crustacea: Anostraca).-American Midland Natural- Brendonck, L. 1995. An updated diagnosis of the ist 109: 55-62. branchipodid genera (Branchiopoda: Anostraca: 1985. A comparison of the gill surface areas of Branchipodidae) with reflections on the genus concept two sympatric species of fairy shrimp (Anostraca, Crus- by Dubois (1988) and the importance of genital mor- tacea).-Freshwater InvertebrateBiology 4: 138-142. phology in anostracan taxonomy.-Archiv fur Hydro- Mura, G. 1986. SEM morphological survey on the egg biologie, Supplement 107 (Monografische Beitrage): shell in the Italian anostracans (Crustacea, Bran- 149-186. chiopoda).-Hydrobiologia 134: 273-286. , M. Hamer, and A. Thiery. 1992. Occurrence of . 1992. Additional remarks on cyst morphomet- tetrahedraleggs in the Streptocephalidae Daday (Bran- rics in anostracansand its significance. Part II: egg mor- chiopoda: Anostraca) with descriptions of a new sub- phology.-Crustaceana 63: 225-246. genus, Parastreptocephalus, and a new species, Strep- Pennak, R. W. 1953. Fresh-water invertebrates of the tocephalus (Parastreptocephalus) zuluensis Brendonck United States.-Ronald Press Co., New York, New and Hamer.-Journal of Crustacean Biology 12: York. Pp. 1-769. 282-297. Thi6ry, A., J. Brtek, and C. Gasc. 1995. Cyst morphol- Brtek, J. 1966. Einige Notizen zur Taxonomie der Fa- ogy of European branchiopods (Crustacea: Anostraca, milie ChirocephalidaeDaday 1910.-Annotationes Zo- Notostraca, Spinicaudata, Laevicaudata).-Bulletin of ologicae et Botanicae, Bratislava 33:1-65. the National Museum of Natural History, Paris, serie . 1967. Eubranchipus (Creaseria) moorei n. 4e, 14: 107-139. sp.-Annotationes Zoologicae et Botanicae, Bratislava RECEIVED:18 February 1997. 36: 1-7. ACCEPTED:13 June 1997. Creaser,E. P. 1930. Revision of the phyllopod genus Eu- branchipus with the description of a new species.-Oc- Addresses: (DB) Biology Department,Our Lady of the casional Papers of the Museum of Zoology, Univer- Lake University of San Antonio, San Antonio, Texas sity of Michigan 208: 1-12. 78207, U.S.A. (e-mail: [email protected]); (GM) Depart- Dexter, R. W. 1946. Further studies on the life history ment of and Human Biology, University La and distribution of Eubranchipus vernalis (Verrill).- Sapienza, Rome, Italy; (SCW) Department of Biology, Ohio Journal of Science 46: 31-44. University of Akron, Akron, Ohio, 44325-3908, U.S.A. . 1959. Anostraca.-In: W. T. Edmondson, ed., Fresh-waterbiology, second edition. Pp. 558-571. John Wiley and Sons, New York, New York.