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JO UR N A L O F CRUST.-\C E.-\N BIOLOGY. 16, 3)' .w ~-~ 5 ~ . 1996

VULNERABILITY OF BRANCHIOPOD CYSTS TO CRUSHING

S. A. Hath away, D . P. Sh eehan, and M. A. Simovich

ABSTRACT Ep hemer al wet lan ds. suc h as verna l pools and pla yas. have become increas ingl y thr eatened by a vari e ty of de structi ve human practices , includi ng off-high way ve hic le (O HV) ac tiv ity. Amo ng the resident ani mals that may be ad versely affec ted are the bra nchiopod crus taceans whi ch produce des iccatio n resi st ant cys ts to withs tand the pools' dry peri od s. We report a qua ntirative investig at ion of the fo rce require d to crush indi vid ua l bran chi op od cysts of 8 spe ­ c ies: Branchin ecta lyn ch i, B. sandie gonen sis. B. ma ckini, St repto cepha lus woouon i, Thamno ­ cephalus platvurus, Linderiella occidentalis, Lep idurus lemmoni, and Tr iops lo ng icaudata . Ver y s ma ll for ces o f less than! new to n crus hed dry cysts. Wet cysts we re even mo re fragile; many were crushed under less tha n 7 x 10-' newtons . Differences in vulnerabi lity were found within and be tween taxa and may be related to cyst morphol ogy. Kn owled ge o f these e ffec ts sho u ld be taken into conside ratio n wh en de ve loping management s trategies for ephe m eral wetlands.

Ephem eral w e tla nds , s uc h as vernal found si gnifi cantly more broken cys ts of pools, playas , and dr y lak es, are deli cate Branchinecta mackini De xter and inc reased systems supporting a rich flora and fauna. breakage of cysts of Thamnocephalus p la­ Man y of the se wetlands are also important tyurus Packar d and Triops longi cau datus to migratory birds and some act as bre eding LeConte in the vehicle tra cks relative to the sites for amphibians. Of the numerou s or­ undisturbed area. ganisms that inhabit ephemeral pools, prob­ In our study, we qu antitativel y measured ab ly the mo st ob viou s are bran chiopod the forces required to cru sh branchiopod cru stacean s, including anostrac an s and no­ cy sts. We also co mpared cyst vulnerability tostracans . These shrimp hatch from desic­ when wet ver sus dry, and tested whether catio n-tolerant cysts (encysted e mbryos) as there were di fference s in the force s required pools fill from rain or ice melt. If co nditions to crush cysts of different spec ies. permit, the y qu ickly mature, mate , and pro­ du ce cysts before the pool dries. The cy sts MATERIALS Ai'iD M ETH ODS remain do rm ant in the so il and ha tch in the We determined the force required to crus h cysts of sa me or subseq uent seasons w hen co ndi­ 6 spe c ies o f an ostracans. Branchinecta lyn chi E ng et tions are again fa vorable. Be cause ephem­ al., 1990. B . sandiego ne nsis Fugate. 199 3, B . m a ckini Dexter, 1956. St repto cep halu s wOOII!)n ; En g et al., eral we tlands are sea so nal, the y are often 19 90 . Thamno ce phalus p latyurus Pack ard, 1879 . Lin ­ overlooked, and ar e becoming increasingly deriella oc cident alis Dobbs, 1923, and 2 species of rar e du e to de structi on from urbani zation, norostr acans. Lepidurus lem m on; Holmes. J894 , a nd agriculture, recreational ac tivities, and other Triops lon g icaudata L inder, t 95 2, from a population now bei ng described as a new s pec ies o f Tr iops (Sas­ ca uses (Eng et al ., 1990). sa man. personal co mmunicatio n). Cysts were co llec ted One particular threat to the remaining fro m dri ed soi l an d intac t cysts we re used d ry or wet natural po ols, playas, an d their inhabitants (af ter ap proxim ate ly 6 h of so aki ng in deio nized wa­ is disturbance fro m off-h ig hwa y vehicles ter). All cysts test ed we re spherical except fo r the 3 species of Branch inecta which had 2 shapes wh en dry. (OHVs). As OHVs pass o ver so il, the either co ncave or s pherica l. Bo th sha pe s are via ble and weight of the vehi cle co mpresses the so il. both we re tested . We tested co ncave cysts to determine Th e largest amount of soil compaction which o rienta tion. sphe ric al si de up or down. was mo re takes place during the first few passes o f durable. We use d the mor e durable or ientatio n. sp he r­ OHVs (Iverson et aI. , 1981), and most com­ ical sid e up , to cal culate crushing force. To de term ine the force required 10 c rush an ind ivid­ paction occu rs just be low the su rfac e ual cys t, a cys t an d a piece o f tun gsten wir e of co m­ (Webb , 1983) Not only is pool hyd rology par able diamete r were pl aced on a m icroscope s lide disrupted by th is act ivity, it is also poten­ equ ally distant from the edge o f the sl ide (Fi g . I). An­ tially very damaging to cysts, most of ot her m icr oscop e sli de was the n ge nt ly res ted o n the wire and the cyst , usi ng fo rce ps . Weight was incre­ wh ich are found in the top few cent ime ters me ntally add ed (us ing for ceps) to the s lide di rectly of so il. Eri kse n et al. (1986) simulated above the cyst unt il it c rus hed. Was hers were used as OHV traffic through a de sert play a and we ights. all owing us to observe cr ushing thr ough the HATHAWA Y IT AL. VULNERABI LITY OF £lRANCHIO PO D CYSTS 44 9

= w e ig h ts RES ULTS Very small forces crushed cysts of all w:JI----=~ species . and there were significant diffe r­ ences between hydrat ion conditio ns and L --- +-I ~ b -- I !-a- I' I among species (F = 85.8. P < 0.000 I) (Figs. 2, 3). When dry, the maximum forc e Fig. I. Diagram of apparatus used to det ermine for ce required to crush even the most resistant required to crus h bran chiopod cysts. dry branchiopod cys ts was less than I ne w­ ton. This is less than the we ight of a 100 g mass. The force was sig nificantly less to center hole . If the cy st c rus hed immed iatel y upon set­ . ting the microscope slide or weight s on the cyst. that crus h wet cy sts of all species (F = 80.7, P test sam ple was thrown out. In case s where more tha n < 0.000 I ) (Figs. 2, 3) . In fac t, 100% of 3 con secutive cysts crushed under the mi cr oscope slide cysts of L. occ ide ntalis, 70% of B . sand ie­ alo ne. the force of the microscope slide wa s used as a g onensis, B. lynchi, and S. wo otton i, and co nser vative estimate of cru shing fo rce . The crushing force (F,,,,,,) for each cys t is: 30 % of B. mackini, crushed unde r the fo rce of the microscope slide alo ne or less tha n 7 F

0.5

0.4

z 0.3

r.'71 l::.:J eo T au ost rac an s > 0.2 < T [2] n ot os tracaos

0.1 T u;

0 B. t. B. m. B. s. L o. S. w. T. p. L l. T. l.

Species

Fig. 2. Average force (N) requ ired to crus h 8 spec ies of branchiopod we t cysts. Values are mean and 95% c.1. (N = 10). Where con fide nce intervals are relat ivel y sm all. no interv al is visibl e in the gra ph . 4 50 JOU RN AL O F CRUSTACEA N BIOL OG Y . V O L. 16. N O . 3. 1996

1.5

z

D an ostr acan s

o not ostr acans

B. I. B. m: B. s. L. o. S. w. T. p. B.,l. B. m B., s. L. L T. L ..".. ( c o nc a v e ) Spe cies

Fig. 3. Average force (N) required to crush 8 species of branchiop od dr y round and d ry co nca ve cys ts. Values are mean and 959'0 C I. (N = to). (Bot h round and conca ve cysts we re found only in the genus Bran ch inecta.) Wh ere co nfide nce interv als are relati vely sma ll, no interva l is visible in the gra ph .

Branchinecta, co mpariso n of concave ver­ This sugges ts th at bran ch iop od cysts can be s us spherical cysts when dr y showed that easily damaged an d are espec ially vulnera­ the concave shape was mo re resistant to . ble when wet. crus hing (t-test = 11.7, P < 0.0001 ) (Fig. Since branchiop od cysts di ffer in topo­ 3). A comparison of concave cysts to sp her­ graphical and internal structu re (Gilc hris t, ical cysts of all anostracan species tested 1978; Mura et al., 1978 ; Mura, 1991; De revealed that concave cysts were signifi­ Walsche et al., 1991; Thiery and Gasc, ca ntly stronger than spheric al cysts, with 1991), it is not unexpected that species dif­ the exception of B . mackinl and T. platyu­ fer in vulnerability to c rushi ng . Cyst Tl/S (F = 1.9, P < 0.05) . Notostracan dr y strength varied with taxa and co nd itio n. No­ cysts were significa ntly more difficult to tostracans are more dur able than anostra­ crus h than concave anos tracan cy sts (F = cans ; thi s is likel y due to an inherently 3.5, P < 0.05), except, howe ver, T. lon gi­ thicker shell wall (T hiery and Gasc, 1991 ). caudatus, which was not sig nificantly dif­ The co ncave s hape o f some dr y cys ts of ferent from B. m ackini. Branchinecta seems to make them on the average three times more s turdy than when DISCUSSION spheric al, in th eir most crush resistant ori­ Sm all forces (less than 1.00 N) we re re­ entatio n. The pe rcentag e o f cysts occurri ng quired to crush eve n the sturdiest cy sts, and in th is state in nature is currently not e ven less force caused crushing when wet. known, nor is th e reason or mechanism fo r fL~ THA WA Y ET AL.: VU LNERABILITY OF B RAN CHIOPO D CY STS 451 the differences in sha pe . Th ere was vari­ quired to crus h cysts on a rigid surface is ability in the cys t stre ngth of a ll spec ies very sma ll. In many a nos tracan species, no t tested. Ou r results are similar to trends all cysts ha tch after a single hyd rati on, pro­ found by Eriksen et al . ( 1986) . Direct co m­ ducing a cyst ban k, co nsisting o f m an y gen­ pari son ca nno t be made , ho we ver, du e to e ra tions . Altho ug h cy st ba nks are lar ge, differences in experimental techniques and p res umably in order to buffer agai ns t pre­ measur ed quantities. They reported pres­ reprodu ct ive losses (Hi ld rew , 1985), it is sure, confo unde d by so il cus hio ni ng, which un kn own what impact repeated loss of a canno t be meaningfully co mpa red to well­ s ignificant portion of a cyst ban k may have characterized fo rces . How ever, both studies o n bran chi opod po pula tions. indicate that not ost racan cysts are more du ­ These find ings have important implica­ rabl e than anostracan cysts. A mo ng the an­ tion s for the co nservation of ephemeral ostraca ns tested when dr y, T. platyu r us was wetlands. We suggest caution sho uld be mo st durable, foll owed by B. mackini (no t taken regarding foot and OHV traffic on sig ni fica nt). Th e resu lts o f Eriksen et al. vernal pools co ntain ing se nsi tive species, ( 1986) for dry-cyst breakage for cysts of T. a nd suc h act ivity may need to be lim ited, pla tyurus approac hed statis tical sig ni ficance particularly during the we t seasons. Fur­ and showed significantly more broken cysts therrnore, curre nt management procedures of B. mackini in soi l co mpress ed by a ve­ (which invol ve sc raping existing pool s to hicle than in the co ntro l sam ple . If the re­ re loc ate soi l that holds plant seeds and an­ sults of Eri ksen et a l. (1986) ca rry over to im al cysts) m ay nee d ree valu ati on . other pool s, it suggests that crus h res is tant spec ies ma y enjoy an evolutionary advan­ ACIGWWLE DGE :V1ENTS tage. Simi larly, it is likely that so me species We th an k Ric ha rd Gonza lez , M ic he l Bo udrias . M i­ will be sig nifican tly more vulnera ble wh en chael Well s . an d De nto n Belk for helpful suggestions. we t. Mor e study is necessary to understand This research was supported in part by a grant from the mechan ism behind spec ies differences th e University of San Diego Associated Students. fo und. L IT ERAT URE CITED Stud ies sho wing the effec ts of OHVs, in­ cl uding those of Iver son et al. ( 198 1) and Belk, D. 1970. Functions of the co nc hostraca n egg she ll.c--Crustaceana 19: 105. Web b ( 1983), have alluded to the d istur­ De Walsche, c., N . Mu nu swamy. a nd H . J . D u m ont. ban ce o f soi ls of verna l pools and, thus, 199 1. S tru ctu ral d ifferences be tween th e cyst walls their inh abitant s, by co mpacting surface of S treptocephalus dichotomus (Baird ), S. to rvico r­ so ils. Not only are cysts in dan ger of out­ n is (Waga), and Thamnoc ephalus p laryurus (Pack­ ard) (C rustacea : A nos traca), and a comparison with right crus hi ng, but also of minor dam age as o the r ge nera and species.-Hydrobio log ia 2 12: 195­ we ll. Bel k ( 1970) found that once desh el­ 202. led , sunlight and mech anical injury place Eng, L. L., D. Bel k. a nd C. H . E riksen. 1990. C al i­ co nchos tracan em bryos (also branchiopods) fornia Anostraca : distrib utio n, ha bitat , and s ta tus .­ in jeopardy. Deshell ed cysts tested re sulted . Jou rn al o f C rus tacean B iolog y 10 : 247-277. Eriksen, C. H., G . E. Prettyman. an d J . E . M o eur. in 60% mortal ity wh en subjec ted to sun ex ­ 1986 . The effects of soil dis tu rba nce by off road posur e and 99% wh en su bje cted to mild vehicles on the eggs a nd ha bi tat o f playa lake c ru s­ abrasion from shaking in sa nd. Man y cys ts t:lceans .- ln: R. G. Zahary, ed .. Desert ecology: a that survive dis turbance with on ly external resea rc h symposium. Pp . 50-65. Southe rn Cali fo r­ nia A cademy of Sciences and Southern California dam age to the cyst shell may later become Dese rt Stud ies C on so rtiu m. Los A nge les, California. inviable fro m sun exposure or san d abra­ G ilch rist. B. M . 1978. Scann ing elec tion mic ro scope sio n. studies of the egg shell in so me Anostraca (Crusta ­ We ha ve fo un d that branchiop od cysts cea: B ran chiopoda).-Cell and Tissue Researc h 193: are vulne rable to crus hi ng on a rigid, static 337-35l. Hi ldre w, A. G . 1985. A q ua ntita tive study of the life s urface. When cys ts are in pool s, soi l par­ of a fairy shrimp (Branchiopoda : A nosrrac a) in re­ ticles surroundi ng them may pro vide cu sh ­ lat ion to the temporary na ture of its habit at , a Ke n­ ioning for so me cys ts, allowi ng g rea ter yan ra inpool.-Jo urnal of A nimal Ecology 54 : 99­ we igh t to be applied before crus hing oc ­ IlO. Iverson, M . R., B. S . Hinc kley, a nd R. M . Webb. 198 1. curs, as is suggested by consideri ng our Physical e ffect s of ve hicular disturbance o n a ri d da ta and those o f Eriksen et a l. ( 1986) D e­ la ndscapes .-Science 2 12: 915-917 . spite this, we have seen that the force re ­ 0 [[. L. 1977. A n introd uctio n to stnr istical metho ds 452 JOUR NAL OF CR UST ACEA N BIOLO G Y. VOL 16. NO. 3. 1996

and analysis.-Pp. 294-298. Duxb ury Press, Bos­ and taxonomi cal value.-Hydrobiologia 2 12: 245 ­ ton, M assachu setts. 259 Mur a, G. 1991. S EM morphology of resting eggs in Webb, R. H. 1983. Co mpaction of desert soils by off­ the s peci es of the ge nus Branch ine cra from North road vehicles.-In: Robert H. Webb and Howard G . America.- Journal of Crustacean Biology 11: 432­ Wils hire. eds. Environmen tal effects of off-ro ad ve­ 436. hicles; impac ts and manage ment in arid regions. Pp. - -- , F. Accordi, and M. Ra rnpini. 1978 . St udi es 5 1- 80 . Sp ringer-Verlag. New York , New York. on the resting eggs of the gen us Chi rocephalus : bi­ RECE tVED: 19 Se ptembe r 1995. ometry and scanning electro n micros copi c mo rphol­ AC CEPTED : 22 Jan uary 1996. ogy (Bra nch iopoda, Anos tracaj.s-i-Crustaceana 35: Ad dr esses: (SAH, MAS) Biology Depart me nt, Uni­ 190- 194 . vers ity of San Diego, 5998 Alca la Par k, S an Diego, T hiery, A., and C. Gasc. 1991. Restin g eggs of An­ Califo rnia 92110, U.S.A.: (DPS) Physic s Department, os traca, No tos traca and Spinicaudat a (C rustacea. University o f San Diego, 5998 Alcala Park, San Diego. Branchiopcda) occuning in Fra nce : identifica tio n California 92110, U.S ,A.