First Record of Fairy Shrimp from Belize, and a Comparison of Cyst-Shell Morphology in the New World Members of the sealii Species Group (: Streptocephalidae) Author(s): William D. Shepard Source: Journal of Biology, Vol. 19, No. 2 (May, 1999), pp. 355-360 Published by: The Crustacean Society Stable URL: http://www.jstor.org/stable/1549242 . Accessed: 17/03/2011 20:54

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http://www.jstor.org JOURNALOF CRUSTACEANBIOLOGY, 19(2): 355-360, 1999

FIRSTRECORD OF FAIRYSHRIMP FROM BFIJ7.E, AND A COMPARISONOF CYST-SHEFI. MORPHOLOGY IN THENEW WORLD MEMBERSOF THE STREPTOCEPHALUSSEALII SPECIES GROUP (ANOSTRACA:STREPTOCEPHALIDAE)

William D. Shepard

ABSTRACT Anostracaare recorded for the firsttime fromBelize, andfor the secondtime fromCentral Amer- ica. The Belizean Streptocephalussimilis occupies a thermalrefuge from insect predators.Cyst- shell morphologiesin the New Worldmembers of the Streptocephalussealii species groupare de- scribed.They indicatea closer relationshipbetween S. sealii and S. woottonithan between either species and S. similis.

While conductingstream surveys in Belize, ter may have offereda refugefrom predation, I found a roadside pond containing a small affirmingthe importantinfluence of physical population of the fairy shrimp Strepto- environmentalfactors upon predation (Wood- cephalus similis Baird. The pond was in a ardand Kiesecker, 1994). While the pondwas forested area of the Rio Bravo Preserve in beside the road,it appearedto be naturaland northernBelize, an area of karsttopography not to be a borrow-ditchresulting from road having much in common with the Yucatan construction.This observationis supported peninsula of Mexico. The collection was by the fact thatroads in this areaare built up made by W. D. Shepardin Belize; Orange by adding crushedlimestone to the existing WalkDistrict, Rio BravoPreserve, in a road- surface, not by using the roadside soil as a side pond 1 mi (1.61 km) south of the head- base. quarterson the east side of the road, 2 Janu- Six of the femaleshad shelledresting-eggs, ary 1996. This collection extends the known or cysts, in their brood pouches. Of the two continentalrange of S. similis approximately that lacked cysts, one had well-developed 1,200 km to the southeast (from southern shell glandswhile the otherdid not. All males Tamaulipas, Mexico). The closest known had readily visible penes. Thus, the popula- population is on Jamaica, approximately tion was evidently reproducing.The total 1,000 km to the east (Moore,1958; Belk, per- lengthsin mm were: males -13.0, 15.5, 17.0, sonal communication).The only other col- 17.5, 19.2, and 19.5; females -14.0, 15.8, lection of anostracansfrom CentralAmerica 16.0, 16.2, 16.2, 17.0, 17.1, and 17.6. (excluding Mexico) is from Costa Rica (Pereiraand Belk, 1987). I collected 14 in- of Streptocephalus.-Early re- dividuals (6 males, 8 females) all of which views of New WorldStreptocephalus are by aredeposited in the collectionof DentonBelk Creaser(1930) and Moore (1966). All spe- (collection numberDB 1272). cies known in Streptocephalusas of 1993 The anostracanswere inhabiting a pond were listed by Belk and Brtek (1995). Three (Fig. 1) filled with potentialinsect predators additionalspecies have been described(Belk (notonectids,nepids, belostomids, and vari- and Brtek, 1997). Maeda-Martinezet al. ous odonate nymphs). Individualsof Strep- (1995a, b) reviewed the systematics of the tocephalussimilis were restrictedto the deep- Streptocephalidaeand split Streptocephalus est partof the pond,and inside extensive beds into nine species groups,three of which oc- of charophyceanalgae. The deepest water, cur in the New World.Their work was based and that inside the algal beds, was cool on adult morphology; cyst characteristics (25?C) compared to the rest of the pond were not used in their analysis. Most of the (30?C). The insects were in the warmersur- pastdescriptive work has involvedadult mor- face watersand on the peripheryof the algal phology. Increasingly,however, attentionis beds. Thus, the algal beds and the cool wa- being given to cysts (Brendonck, 1989; De

355 356 JOURNALOF CRUSTACEANBIOLOGY, VOL. 19, NO. 2, 1999

Fig. 1. Roadside pond with charophycean algal beds occupied by Streptocephalus similis.

Walsche et al., 1991; Mura, 1992a, b). Cyst illustrated,but did not systematically describe, morphology has been used to make identifi- cyst exteriors for all three New World S. sealii cation keys for regional groups of Strepto- group species. Considerable interspecific cephalus spp. (Brendonck and Coomans, variation in cyst size has been found in S. 1994a, b). It has become important in de- sealii (Belk et al., 1990). Some of that vari- scriptions of new taxa to include descriptions ation is related to female size and some to of cysts (Brendonck et al., 1992; Brendonck variables. Some may be due to un- and Belk, 1993; Hamer and Brendonck, 1993). known cryptic species. Research into cyst Most cyst illustrations and/or descriptions variation in S. sealii is being initiated have dealt only with cyst exteriors. Only re- (Richard Hill, personal communication). cently has there been examination of the in- The interior and exterior morphology of terior of cyst shells. Cyst-shell cross sections cysts of S. sealii and S. woottoni have been have been illustrated for S. dichotomous studied as part of a study of cysts in Califor- (Baird) (see De Walsche et al., 1991) and S. nia anostracans(Hill and Shepard, 1997). With texanus Packard (see Hill and Shepard, 1997). the collection of cyst-bearing females of S. The S. sealii species group is comprised similis, in was possible for me to examine all of three New World species (S. sealii Ryder, the New World species in the S. sealii species S. similis Baird, S. woottoni Eng, Belk and group. In doing so, I hoped to determine Eriksen; see Appendix for collection records) whether cyst morphology is as useful as adult and three Old World species (S. bourguinii morphology (Maeda-Martinez,1995a) indicat- Hamer and Appleton, S. distinctus Thiele, S. ing relationshipsamong closely related species. spinosus Daday) (Maeda-Martinez et al., 1995a). Brendonck and Coomans (1994b) MATERIALSAND METHODS have illustrated and described systematically The Belizean fairy shrimp were preserved in 70% iso- cyst exteriors for the Old World species S. propyl alcohol in the field and later switched to 70% ethyl distinctus and S. spinosus. Mura (1992a) alcohol. In the laboratory, cysts were removed from one

Figs. 2-7. Cysts of Streptocephalus. Fig. 2. Streptocephalus sealii, whole cyst. Scale bar = 50 gm. Fig. 3. Strep- tocephalus sealii, cyst wall cross section. Scale bar = 10 gJm. Fig. 4. Streptocephalus similis, whole cyst. Scale bar = 20 gm. Fig. 5. Streptocephalus similis, cyst wall cross section. Scale bar = 10 gm. Fig. 6. Streptocephalus woot- toni, whole cyst. Scale bar = 50 gm. Fig. 7. Streptocephalus woottoni, cyst wall cross section. Scale bar = 5 gum. SHEPARD:STREPTOCEPHALUS FROM BELIZE 357 358 JOURNALOF CRUSTACEANBIOLOGY, VOL. 19, NO. 2, 1999 female for examination by scanning electron microscopy of the alveolar layer. Cysts of S. sealii lack (SEM). Egg preparation followed that of Hill and Shep- the larger columnar supports and thus have ard (1997). Terminology for internal structures follows that of Lee et al. (1994) and Hill and Shepard (1997). none of the large hollows found in the alve- Eggs of S. sealii Ryder and S. woottoni Eng, Belk, olar area of S. woottoni. and Eriksen were obtained from alcohol-preserved mu- seum from four each of S. specimens. Eggs populations DISCUSSION sealii and S. woottoni were examined. Specific collec- tion data are listed in the Appendix. The habitat of the Belizean population sug- With the use of SEM, the entire cysts were pho- gests that S. similis may be located in the Yu- and a cross section of the tographed cyst shell, together catan of searches with any unusual surface structures (Hill and Shepard, peninsula Mexico, although 1997). The diameter of several cysts per population was there have not found this species. The Be- measured using an in-scope micrometer. lizean population greatly reduces the previ- ously known large disjunction (between Ja- RESULTS maica and Tamaulipas,Mexico) between pop- ulations of S. similis. No birds are known to For the populations examined, I found con- migrate between these populations and sistent differences in cyst morphology among thereby serve as vectors between the disjunct members of the S. sealii species group. Indi- populations. However, this new population vidual cyst diameters per female are listed in adds to the trajectory that suggests movement the Appendix. Composite descriptions from of the fairy shrimp via plate tectonics the populations examined are as follows. (Maeda-Martinez et al., 1995a). Externally, cysts from all known members The external shape of the cysts in the mem- of the S. sealii group are spherical with large bers of the S. sealii group is typical for all rugosities defining polygonal depressions New World species and some Old World spe- 2, 4, 6). (Figs. cies (excluding the subgenus Parastrepto- Streptocephalus sealii (Figs. 2, 3).-Cyst di- cephalus Brendonck, Hamer, and Thiery, ameter 236-307 igm (x= 274, N = 19, 3 pop- which has tetrahedral cysts). The internal ulations). Cortex relatively thick (-5 gm) and cyst-shell morphology falls within the vari- solid, with few pores. Alveolar layer com- ability already described for cysts of Strep- posed of short anastomosing branches defin- tocephalus. ing numerous small vesicular hollows. Ter- In respect to cyst morphology, S. sealii and tiary base relatively thin. S. woottoni appear to be more closely related to each other than either is to S. similis. This Streptocephalus similis (Figs. 4, 5).-Cyst di- fits the proposal by Maeda-Martinez et al. ameter 190-200 Rim(x= 196; N= 10; 1 pop- (1995a) of "working hypothesis for the phy- ulation). Cortex relatively thin (-2.5 gm), logeny of New World species." However, nei- with pores numerous on flat ridge tops. Alve- ther matches their cladogram for Strepto- olar layer composed of inner sublayer of nu- cephalus worldwide, which shows S. woot- merous short anastomosing branches defining toni less closely related to the species pair S. small vesicular hollows, and outer sublayer sealii/S. similis. of columnar supports in predominately open space. Tertiary base relatively thin. ACKNOWLEDGEMENTS Streptocephalus woottoni (Figs. 6, 7).-Cyst Denton Belk provided many helpful comments and en- read two earlier drafts. diameter 240-310 = 268, N = 30; 3 couragement, and critically gm (x Richard Hill provided helpful comments and much valu- populations). Cortex relatively thick (=5 gm) able assistance. I thank Earl Green and Rafael Manzanero and solid, with few pores. Alveolar layer with (Department of Forestry, Belize) for approving permits to mixed areas of short anastomosing branches conduct aquatic surveys in Belize, and The Program for defining small vesicular hollows, and colum- Belize for permission to collect at the Rio Bravo Preserve. nar supports defining large hollows. Tertiary base relatively thin. LITERATURECITED Cysts of S. similis are readily distinguished Belk, D., and J. Brtek. 1995. Checklist of the Anos- from those of S. sealii and S. woottoni by traca.-Hydrobiologia 298: 315-353. their smaller size and thinner cortical , and . 1997. Supplement to 'Checklist of layer. the Anostraca'.-Hydrobiologia 359: 243-245. Cysts of S. sealii and S. woottoni are gener- , G. Anderson, and S.-Y. Hsu. 1990. Additional ally very similar, but differ in the structure observations on variation in egg size among popula- SHEPARD:STREPTOCEPHALUS FROM BELIZE 359

tions of Streptocephalus seali (Anostraca).-Journal of Lee, W. K., M. A. Gouthro, D. Belk, and J. R. Rosowski. Crustacean Biology 10: 128-133. 1994. Ultrastructure features of the tertiary envelope Brendonck, L. 1989. Redescription of the fairy shrimp in the cyst of the brine shrimp Artemia franciscana Streptocephalusproboscideus (Frauenfeld, 1873) (Crus- (Anostraca).-In: G. W. Bailey and A. J. Garratt-Reed, tacea, Anostraca).-Bulletin de l'Institut Royal des Sci- eds., Proceedings of the 52nd meeting of the Mi- ences Naturelles de Belgique, Biologie 59: 49-57. croscopy Society of America. Pp. 362-363. San Fran- , and D. Belk. 1993. Streptocephalus coomansi, cisco Press, San Francisco, California. a new fairy shrimp species (Crustacea: : Maeda-Martinez, A. M., D. Belk, H. Obreg6n-Barboza, Anostraca) from Kenya.-Journal of African Zoology and H. J. Dumont. 1995a. Diagnosis and phylogeny 107: 535-541. of the New World Streptocephalidae (Branchiopoda: , and A. Coomans. 1994a. Egg morphology in Anostraca).-Hydrobiologia 298: 15-44. African Streptocephalidae (Crustacea: Branchiopoda: 9, , , and . 1995b. A contri- Anostraca) Part 1: South of Zambezi and Kunene bution to the systematics of the Streptocephalidae rivers.-Archive fur Hydrobiologie, Supplement 99: (Branchiopoda: Anostraca).-Hydrobiologia 298: 313-334. 203-232. , and . 1994b. Egg morphology in African Moore, W. G. 1958. On the occurrence of Strepto- Streptocephalidae (Crustacea: Branchiopoda: Anos- cephalus similis Baird in Mexico and the United traca) Part 2: North of Zambezi and Kunene rivers, and States.-Journal of the Washington Academy of Sci- Madagascar.-Archive fur Hydrobiologie, Supplement ences 48: 169-175. 99: 335-356. . 1966. New World fairy shrimps of the genus , M. Hamer, and A. Thi6ry. 1992. Occurrence of Streptocephalus (Branchiopoda, Anostraca).-South- tetrahedraleggs in the Streptocephalidae Daday (Bran- western Naturalist 11: 24-48. chiopoda: Anostraca) with descriptions of a new sub- Mura, G. 1992a. Pattern of egg shell morphology in genus, Parastreptocephalus, and a new species, Strep- thamnocephalids and streptocephalids of the New tocephalus (Parastreptocephalus) zuluensis Brendonck World (Anostraca).-Crustaceana 62: 300-311. and Hamer.-Journal of Crustacean Biology 12: . 1992b. Additional remarks on cyst morpho- 282-297. metrics in anostracans and its significance. Part II: egg Creaser, E. P. 1930. The North American phyllopods of morphology.-Crustaceana 63: 225-246. the genus Streptocephalus.-Occasional Papers of the Pereira, G., and D. Belk. 1987. Three new species of Museum of Zoology, University of Michigan 9(217): Dendrocephalus (Anostraca: Thamnocephalidae) from 1-10. Central and South America.-Journal of Crustacean De Walsche, C., N. Munuswamy, and H. J. Dumont. Biology 7: 572-580. 1991. Structuraldifferences between the cyst walls of Woodward, B. D., and J. Kiesecker. 1994. Ecological Streptocephalus dichotomus (Baird), S. torvicornis conditions and the notonectid-fairy shrimp interac- (Waga), and Thamnocephalus platyurus (Packard) tion.-Southwestern Naturalist 39: 160-164. (Crustacea: Anostraca), and a comparison with other genera and species.-Hydrobiologia 212: 195-202. RECEIVED:4 February 1998. Hamer, M., and L. Brendonck. 1993. A new species of ACCEPTED:4 August 1998. Streptocephalus (Crustacea, Branchiopoda, Anostraca) from Namibia.-Annals of the South African Museum Address: Departmentof Entomology, California Acad- 103: 183-189. emy of Sciences, Golden Gate Park, San Francisco, Cal- Hill, R. E., and W. D. Shepard. 1997. Observations on ifornia 94118, U.S.A. (Mailing address: 6824 Linda Sue the identification of California anostracan cysts.-Hy- Way, Fair Oaks, California 95628.) (e-mail: sl2647@ drobiologia 359: 113-123. saclink.csus.edu) 360 JOURNALOF CRUSTACEANBIOLOGY, VOL. 19, NO. 2, 1999

APPENDIX. COLLECTIONDATA FOR THREE side of road, 2 January 1996, W. D. Shepard, collec- = 15.8 mm total diameters SPECIESOF STREPTOCEPHALUS. tor. Female length. Cyst measured (in gim): 190, 190, 194, 196, 196, 196, 199, Streptocephalus sealii, females 199, 200, and 200. SSEL1-California: Tuolumne County, Kole Lake, 8,500 Streptocephalus woottoni, females ft. (2,593 m) elevation, 21?C, 31 July 1989, Brian SWO1-California: Riverside Skunk Hollow, Quelvog, collector. Female = 17.0 mm total length. County, south basin, 33?34'N, 117?06'W, 1,340 ft. (409 m) el- Cyst diameters measured (in jim): 261, 266, 270, and num- 307. evation, 19 March 1992, C. Eriksen, collector, ber A2-122. Female = 11.2 mm total length. Cyst di- SSEL2-California: Tehama County, 40?25'N, 121?35'W, ameters measured (in jim): 240, 243, 243, 245, 246, 7,150 ft. (2,972 m) elevation, 23 June 1987, Clyde Erik- 247, 250, 254, 257, and 257. sen, collector, number A2-134. Female = 13.0 mm to- SW02-California: Riverside County, Pala Road, 23?C, tal length. Cyst diamters measured tin gim): 236, 240, 19 March C. number A2-187. 247, 257, 261, 268, 268, 278, 282, and 289. 1992, Eriksen, collector, Female = 13.3 mm total length. Cyst diameters mea- SSEL3-California: Siskiyou County, "Newt Wallow," sured (in jim): 261, 264, 268, 268, 271, 275, 275, 275, Klamath Mountains, Dillon Divide near County Line, 278, and 310. 10 August 1985, G. Newton, collector. Female = 17.5 SW03-California: Riverside across road from mm total length. Cyst diameters measured (in ,um):282, County, Skunk 19 March C. col- 282, 282, 285, and 285. Hollow, 28?C, 1992, Eriksen, lector, number A2-186. Female = 9.5 mm total length. SSEL4-California: Lassen County, 26 km north of Su- Cyst diameters measured (in jim); 271, 275, 278, 278, sanville, 1 July 1986, Ed. Smith, collector, California 282, 282, 282, 282, 289, and 307. Academy of Sciences collection. No cysts measured. SW04-California: San Diego County, bluffs above Streptocephalus similis, female White Beach, Camp Pendleton, Pool A, 23 March 1993, J. E. collector, number M23Mar93-5. Female Belize: Orange Walk District, Rio Bravo Preserve, in road- Moeur, = 28.0 mm total No diameters measured. side pond, 1 mile (1.61 km) south of headquarters,east length. cyst