host fishes and infection strategies of freshwater mussels in … · 2013-12-08 · host fishes and...

Host fishes and infection strategies of freshwater mussels in largeMobile Basin streams, USA

WENDELL R. HAAG' AND MELVIN L. WARREN, JR.USDA Forest Service, Southern Researck Station, Center for Bottomland Hardxuods Researck,

1000 Front Street, Ox&d, Mississippi 38655 LISA

Abstract. We investigated host fishes, timing and modes of glochidial release, and host-attractionstrategies for 7 species of freshwater mussels from the Buttahatchee and Sipsey rivers (Mobile Basin),Alabama and Mississippi, USA. We determined hosts as fish species that produced juvenile musselsfrom laboratory-induced glochidial infections. We established the following primary mussel/hostrelationships: Elliytio nrcn with Etl~~~tomu nrtcsinc and Percitza ~zigr#scintu; Fusconain cerina with 6species of minnows (Cyprinidae); Lm7psilis ormtn with Micropkrus sahoidcs; Mcdionidus acutissimuswith 8 species of darters (Percidae); Obtnwrin unicolor with Anrmmytn bcnili, A. nrcridinrm, and Et/l-enstomn art&v; Phrobemn decisunr with Cyril~elln wrmstn; and Quadruin aspernta with lctnlurus punt-tatus. For most mussel species, host use was similar to that of closely related species, indicating that,in general, this trait is highly conserved at the generic level. Four mussel species used host-attractionstrategies that targeted their specific host fish. Fusronnin cerirla and I! dmisurn released glochidia inconglutinates that elicited feeding responses from fishes in the field and in the laboratory. Gravidfemale Dmrpsilis ornatn and M. ncutissimus displayed mantle lures. Host-attraction strategies were lessapparent for E. arcn and (2. nspmdn, but these species released glochidia in association with copiousmucous secretions, which may serve to entangle fishes, facilitating host infection. No host-attractionstrategy was apparent for 0. uiiicolor.

Kr?/ zards: host-parasite relationship, life history, Unionidac, Bivalvia, mussels, glochidia, MobileBasin.

The southeastern United States supports themost diverse freshwater mussel fauna on earth.This fauna also is distinguished as one of themost endangered groups of organisms in NorthAmerica (Neves et al. lYY7). The basic life his-tories of many southeastern mussel species arepoorly known. To complete development, larvae(glochidia) of most mussel species must under-go a brief period as ectoparasites on the gills orfins of fishes. Host specificity ranges from gen-eralists, able to parasitize a wide variety of fish-es, to specialists, whose glochidia can developon only a few, usually closely related fish spe-cies (Haag and Warren 1997). Larvae cncounter-ing an unsuitable host are rejected by the fishimmune system (O’Connell and Neves 1099).Many species display remarkable adaptations tofacilitate transmission of glochidia to hosts, in-cluding display of lures and release of glochidiain packets that mimic food items of host fishes(e.g., Barnhart and Roberts 1997, Haag and War-ren lYYY, Watters 1999, Jones and Neves 2002).Knowledge of host fishes, host-attraction strat-egies, an d other aspects of reproductive biologyis lacking or incomplete for many North Amer-

ican mussel species. This lack of knowledgehampers conservation efforts and limits our un-derstanding of the ecology of these animals.

The Mobile Basin of Alabama, Georgia, Mis-sissippi, and Tennessee is home to a unique,highly endangered mussel fauna including alarge number of endemic species (Stansbery1976, Lydeard and Mayden 1995). The Butta-hatchee and Sipsey rivers support the best re-maining examples of large-stream Mobile Basinmussel communities. Host information exists fora number of headwater species in the MobileBasin (Haag and Warren 1997, Haag et al. 1999),but hosts are unknown for most large-streamspecies in the basin.

We investigated host fishes, timing andmodes of glochidial release, and host-attractionstrategies for 7 species of mussels from the But-tahatchce and Sipsey rivers: Alabama spike (EI-liptio nrcn), Gulf pigtoc (Fuscouaia cerina), south-ern pocketbook (Laqwilis orunto), Alabamamot casinshell (MeJiorlidus achssimus), Alabamahickorynut (Obtn~~7rin frrricoh), southern club-sheii (I’lrlrlobc~~rn dccimm), and Alabama orb(Q~rrrdmln nsprnrtn). With the exception of E C~V-irla and L. ormta, all of these species are endemic

78

20031 MUSSEL HOSTS AND INFECTION STRATEGIES 79

to the Mobile Basin. Fz~sconnia ceri~~n also occursin the Amite, Pearl, and Pascagoula rivers (Wil-liams and Fradkin 3 999), and L. ornntn is endem-ic to Gulf of Mexico drainages from the AmiteRiver east to the Escambia River (Williams andButler 1994). The US Fish and Wildlife Servicerecognizes I? &cist~~~ and M. acutissimus as en-dangered and threatened, respectively. TheAmerican Fisheries Society considers E. nrcnthreatened, and L. ornatn, 0. unicolor, and Q. as-per&a species of special concern (Williams et al.1993). Along with 2 other species not studiedhere (Q&rula rumphinna and Tritogonia uerru-cclsa), these 7 species dominate mussel commu-nities in the Buttahatchee and Sipsey rivers(WRH and MLW, unpublished data).

Methods

We determined host fishes by inducing glo-chidia l infestat ions in laboratory t r ia ls and mon-itoring the rejection of glochidia or productionof juvenile mussels. Our methods were de-scribed by Haag and Warren (1997) and arebased on a standard host- identi f icat ion protocol(Zale and Neves 1982). We identified primaryhost-fish species as those that consistently pro-duced live juvenile mussels. We identified un-suitable host-fish species as those in which allmussel g lochidia were re jected from al l individ-ual fishes without producing juvenile mussels.In some cases, some individuals of a particularfish species rejected all glochidia, but othersproduced juvenile mussels . Because of inconsis-tent glochidial transformation, we regardedthese fish species as marginal hosts. For cac11mussel species , we ran 2 to 4 repl icate tr ia ls (20-22”C), us ing glochidia f rom a di f ferent female ineach tr ial . We exposed glochidia from each mus-sel species to 15 to 34 fish species (l-10 individ-uals of each). We chose fish species to representmost families and genera and all common spe-cies present at study sites (Boschung 1989).

We col lected gravid female mussels f rom theButtahatchee River, Monroe Co., Mississippiand the Sipsey River, Pickens/Greene Co., Ala-bama in June and J~tly 1998 and 2001. Bothstreams are large tributaries of the TombigbeeRiver (Mobile Basin). Water temperature at thetime of collection was 22 to 30°C. We collectedmussels by diving and, in shallow areas, bysearching the stream bottom using a glass-bot-tomed bucket. We assessed reproductive status

of each individual by gently prying apart thevalves and examining the gills. We recognizedgravid females by the presence of distendedgills. We immediately returned male and non-gravid specimens to the stream. We broughtgravid mussels into the laboratory and placedthem into individual, aerated beakers at roomtemperature (21-25°C). Most individuals of E.urea, E ccrinn, I! decisum, and Q. nsperata releasedglochidia into the beakers within 24 to 48 h; weused these glochidia in host trials immediatelyupon release. Lnmpsilis orrlntn, M. acutissimus,and 0. u~zicolor did not release glochidia in thelaboratory. With the exception of P deciszrl~z andM. acutissimxs, we harvested glochidia from in-dividuals that did not release in the laboratoryby sacrificing the animal and dissecting thegills. WC harvested glochidia from M. ncutissi-rnzls by flushing the contents of the gills into abeaker using a hypodermic syringe and agedtap water. Because of their federal conservationstatus, M. aczrtissimus and l? decisum were re-leased alive where they were co l lec ted wi th in 7d of col lect ion. We worked with these 2 speciesunder US Fish and Wildli fe Service EndangeredSpecies Subpermitee Authorizat ion Number SA-98-06, Mississ ippi Department of Wildl i fe , F ish-er ies , and Parks Scient i f ic Col lect ing Permit , andAlabama Department of Conservat ion Sc ient i f i cCollect ing Permit Number 182.

We based descr ipt ions of gravid per iods on acomposi te of f ie ld observat ions f rom 3 996, 1998,2000, and 2001; we based descriptions of host-attraction strategies and glochidial release onfie ld and laboratory observat ions f rom the sameperiod. We classified species into 1 of 2 catego-ries , short - term or long- term brooders , based onthe duration and timing of the gravid period(Kat 1984). We used glochidia from gravid fe-male mussels f rom the fo l lowing loca l i t ies anddates in host - ident i f icat ion t r ia ls ( t r ia ls are iden-tified as A, B, C, or D): Alabama-Sipsey River,Pickens-Greene Co.: E. arca, A, 6 July 1998, B, 27June 2001; E crrirza, A, 10 June 1998, B, 8 July1998, C, 29 July 1998; L. orrznfa, A and B, 6 July1998; 0. urzicolor, A, 17 June 1998, B, 26 June1998, C and D, 27 June 2001; I! ciecis44n4, A, 14July 1998, B, 29 July 1998, D, 3 July 2001; Q.nsprrntn, A, 26 June 1998, B, 14 July 1998; Mis-sissippi-Buttahatchee River, Monroe Co.: Eccrina, D, 22 June 2001; L. orllata, C and D, 28June 2001; M. acutissimus, A, 21 June 2001, B, 28June 2001; (2. ilspcrata, C, 22 June 2001. We de-

80 W . R . HAAG A N D M. L. WAMEN [Volurne 22

TAMI.I: 1. Results of host trials for Elliptic RITZ. Letters A and I3 rcpresent replicate trials using glochidia from2 different female mussels. Sample size (n) is either the number of fish that produced juvenile mussels or thenumber of fish that rejected all glochidia and produced no juvenile mussels. - = the fish species was not usedin the trial. na = not applicable.

Mean no. juveniles/fish (II)

Fishes’

Days to transformation

A B

Days to rejection (n)

A B

Hosts8 (3)

19-295 (2)

15-19

9 (3)22-35

-

na (0)

na (0)

na (0)

-

- 3 (1) - 4 (1)33

’ Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not producejUVellih2 mUSSelS: ~~i~y~kpis (1, 3, 2), cI&V’ilZC/k? W?US~? (2, 4.5, 2-2(l), hxihs c/i~!/socc~~,~m~us (1, 4, 2-7),~@‘fu’f~s bdhfs (1, 4, 4), L. ~rrrdV’~ti/is (1, 2, 2), Notm~@nftS C,‘~JSOkWci?S (2, 3, Z-7), hbtroy~is nrmrophihs (2, 3.5, 2-4),N. nthiuoid~S (1, 2, 2-20), N. Imikq~i (1, 2, Z-7), N. stilbifrs (1, 3, 4), N. ahcdhs (1, 2, 2), Pi~~rqhnks mtntus (1, 4, 2),Icfiohs hbnhrs (1, 2, 2), Irtolrrrus pmfntus (2, 2, Z-5), Notw~rs k~pfncnizthus (1, 2, Z-14), Lqmris cy~lnndhrs (2, 2, 5-14), 1,. mm’ochir~rs (1, 2, 7-14), L. myhtis (2, 2.5, 2-7), Microptcrus sn2md’s (2, 3, 7-lY), Anmoctypfa b~nt~i (1, 2,4), Efheosformi ryesfw (2, 2, 2-4), E. sti<~mrrcwi~~ (I, 3, 4-39)

posited voucher specimens of all species at theMississippi Museum of Natural Science(MMNS), Jackson, Mississippi and the IllinoisNatural History Survey, Champaign, I l l inois .

We collected most potential host fishes fromthe fol lowing streams in the western Mobile Ba-sin: Alabama-Clear Creek (Black Warrior Riv-er system), Winston Co.; Mississippi-BullMountain Creek (Tombigbee River system), Ita-wamba Co.; Noxubee River (Tombigbee Riversystem), Winston Co.; Hashaqua Creek (Tom-bigbee River system), Noxubee Co. We aug-mented f ish col lect ions with specimens from thefollowing streams: Alabama-Cedar Creek(Tennesee River system), Franklin Co.; Missis-sippi-Goodwin Creek (Yazoo River system),Panola Co.; Lee Creek (Yazoo River system), La-fayette Co. ; and Litt le Tallahatchie River (YazooRiver system), Lafayette Co. We collected allfishes from stream sites without mussels orwith low mussel densities to avoid using fishwith pre-existing glochidial infestations or ac-quired immunity to glochidia (Zale and Neves1982). We obtained Ictnlnrus punctatus, Micrcpterrrs snln~)i&s, and Notmzi~mus crysolcuc~zs fromhatchery stock. We maintained al l f ishes in aer-ated aquaria in the laboratory and fed thembloodworms (minnows, darters, madtoms),

earthworms and minnows (sunfishes), and pel-let ized f ish food (channel catf ish) .

Results

El l ip t io arca

El l ipf io ~IYCIZ is a short-term brooder and wasgravid from late spr ing to ear ly summer. We ob-served gravid female E. arca from 28 May to 28July and mature glochidia from 27 June to 28July. In the laboratory, mature glochidia were re-leased freely and were not contained in conglu-tinates. Some glochidia were released in smallclusters that disassociated quickly af ter re lease .Copious mucus was released with mature glo-chidia, and many glochidia were bound in thismucus. Long strands of mucus often issuedfrom the excurrent s iphon of re leas ing females .Immature glochidia and eggs were released inirregular clusters, which conformed loosely tothe shape of the gill water tubes. These clustersresembled true conglutinates (see E cuina) butlacked a regular, cohesive shape, and never con-tained mature glochidia.

Glochidia of E. arca transformed consistentlyon only 2 darter species (Percidae): Efhcosfomnnrfrsiae and krcinrr nigrqf iwiofa (Table 1). Glo-

82 W. R. HAAG AND M. L. WARIXEN [Volume 22

schools of blacktail shiners, Cyprinella venusta,repeatedly approaching drifting conglutinates.Because of the fishes’ rapid movements, wecould not discern whether shiners ingested con-glutinates; in most cases, the fishes approachedconglutinates very closely and then veered offjust before , or at , the moment of contact . I f shin-ers did ingest conglutinates, contact was brief,and conglutinates were expelled quickly. In thelaboratory, we presented conglutinates to min-nows (C. vemsta, Nocolnis leptocepkulus, and No-fropis ammopkilus), darters (Etkeostoma rupestrcand Percina sciera), and sunfish (Lepomis macro-ckirus). All fish species responded to the pres-ence of conglutinates by repeatedly approachingthem closely as observed in the f ie ld, but again,in most cases, we could not discern if individ-uals ingested conglutinates . We observed an in-dividual of E. rupestre ingest and expel a con-glutinate 3 times in rapid succession.

Glochidia of E cerina transformed on a widevariety of minnow species (Cyprinidae) (Table2) . Glochidia t ransformed consis tent ly on 6 min-now species and inconsistently on 6 additionalminnow species . Five minnow species were un-suitable hosts. Fourteen other fish species, rep-resenting the families Catostomidae, Centrar-chidae, Ictaluridae, and Percidae, were unsuit-able hosts for E cerina (Table 2).

Lampsi l i s ornata

Lampsilis ornata is a long-term brooder andwas gravid from late summer to late spring ofthe fol lowing year . We found gravid individualsthroughout most of the year with the exceptionof July to September when most females werespent. Lampsilis ornata did not release glochidiain the laboratory. Gravid females displayed alarge mantle lure that we observed in the labo-ratory and in the field. The lure consisted of apair of elongated flaps e-50 to 75 mm long,which protruded beyond the shel l margin, withthe gravid gills visible between the flaps. Eachflap was cream colored with a distinct eyespotand a dark, lateral stripe, and flaps were pul-sated vigorously during display. The lure anddisplay behavior closely resembled that de-scribed for L. cardiwn (Kraemer 1970, Haag andWarren 1999).

Glochidia of L. ornata transformed only onlargemouth bass , Micro~~trrtrs sa lmoides (Centrar-chidae) (Table 3) . Four centrarchid species were

unsuitable hosts. Ten other fish species, repre-senting the famil ies Catostomidae, Cyprinidae,Esocidae, Ictaluridae, and Percidae, were unsuit-able hosts for L. ornata (Table 3).

Medionidus acutissimus

Medionidus acufissinzus is a long-term brooderand was gravid from approximately October toJune of the fol lowing year . By late May, gi l ls ofmost females had only 2 to 3 gravid water tubes(fully charged gills have -3040 gravid watertubes) . Most females were spent from early JUneto October . Females did not re lease glochidia inthe laboratory. We observed several gravid fe-males in the Sipsey and Buttahatchee r ivers dis-playing smal l , b lack modif ied mantle margins .When displaying, females were widely agapeand completely unburied but were often lyingwithin the in ters t i ces o f coarse gravel or cobblesubstrates in swift currents. Females usuallywere tethered to a pebble by a byssal thread.We observed displaying individuals in a varietyof or ientat ions with the dorsal margin facing up,the ventral margin facing up, or lying on theirside. The modified portion of the mantle ex-tended along the ventral margin of the shellf rom the poster ior t ip to s l ight ly anter ior o f themidpoint of the shell . The modified mantle wasmatte, inky black with a small (-2 mm2), whitepatch located at about the midpoint of the shel l ,near the anterior-most portion of the modifiedmantle margin. The white patch flickered rap-idly at -1 s intervals; the motion was similar tothe f l icker ing of a te levis ion screen. With the ex-ception of the flickering mantle patch, display-ing females appeared moribund and showed l i t -tle response to handling. Females remainedwidely agape when removed from the water,and did not attempt to close the shell or retractthe mantle margins . The f l icker ing motion of thewhite patch often continued for 15 s or moreafter being removed from the water. These be-haviors were not observed in the laboratory.

Glochidia of M. acutissimus transformed on awide variety of darter species (Percidae) (Table4). Glochidia transformed consistently on 8darter species. Another darter species, E. ruyes-tre, was a marginal host . No darter species wereidentified as unsuitable hosts. Seven fish spe-cies, representing the families Centrarchidae,Cyprinidae, and Ictaluridae, were unsuitablehosts for M. acutissirmts (Table 4).


TAIXT 2. Results of host trials for Fwco~zai~ c&m. Letters A to D represent replicate trials using glochidiafrom 4 different female mussels. Sample size (71) is either the number of fish that produced juvenile mussels,or the number of fish that rejected all glochidia and produced no juvenile mussels. * = all fish died beforecompletion of the trial. - = the fish species was not used in the trial. na = not applicable.

Mean no. juveniles/fish (n)

Fishes’

Days to transformation Days to rejection (II)

A B C D A B C D

-

*-

*

-

*

0 (f-3n a

0 (0)n a-

-

*

20)1 5

2 (2)19-21

-

15 (7)19-26

-

1 (3) o* (3)19-21 1 5

- -

2 (4)14-21

0 (0)L

“Yb)‘

0;)n a

7 (1)2 1-

0 UNna

2 (3)14-161* (1)

1 44 (3)

14-19-

I* (3)1 4

6 (4)24-3222 (1)

241 (1)20

3 (3)24-31

2 (3)27-31

1 (1)18-27

1 (4)18-27

2 (1)1 8

1 (2)20-240 (0)

2nF3)18-26

-

- na (0) -

* na (0) na (0)

-

na (0) na (0)

-

- na (0)

* 2 (4) 5-7 (2)

2 -5 ( I ) 5 (2) na (0)

2 (2) 2-14 (3) 13 (1)

- 2 (2) -

- -

* 2-20 (3) 12 (1)

na (0)

na ( 0 )

na ( 0 )

na (0)

na (0)

na (0)

3 (1)

3 (1)

3 (1)

3 (1)

3-6 (2)

-

’ Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not producejuvenile mussels: Ffybr~,~f?~zth~~s ~~whnlis (2, 1, 5-18), Nofropis bnikyi (2, 4.5, l-12), N. ksn~zus (1, 5, 2), N. whrcrlhrs(2, 3, 2-3), Pimcplralcs zilgilm (7, 3, 3), Icfiobus bubnlns (I, 2, 2), Rvburus mtnlis (1, 2, 5), Ictnlurus pumdfus (2, 3,3-5), Notfirus Ir~ptacnrzths (1, 3, 5), Lqmwis cymelhs (1, 3, 2-5), L. mmdGm (2, 2.5, 2-12), L. meCgokdis (3, 2.3, 2-3), Micropferus snlmoides (3, 2.5, 2-7), Po~rmxf:: nrlmrlaris (1, I, 5), Etheostolnn wtmim (2, 3, 5-7), E. rzqvstre (3, 4.3,l-7), E. stigumcrcrn (1, 3, 3), Pcercinn rligrofmintm (2, 3.5, 2-18), i? scim (I, 2, 2-7)

Obovaria unicolor

Oboumk zmicokv is a long-term brooder andwas gravid from approximately August to Juneof the following year. Glochidial release tookplace from April to June. We observed fullygravid and partially spent females from Aprilto early June. After 8 June, we found only par-tially spent individuals and, after 26 June, allfemales were completely spent. By late August,we found gravid females that were broodingembryos. We observed gravid females with ma-

ture glochidia by November. Females did not re-lease glochidia in the laboratory, and we ob-served no mantle displays in the field or labo-ra tory .

Glochidia of 0. ~nicolou transformed consis-tently on 3 darter species (Percidae) and incon-sistently on 4 addit ional darter species (Table 5) .Six darter species were unsuitable hosts. Twen-ty other fish species, representing the familiesCatostomidae, Centrarchidae, Cyprinidae, Eso-cidae, and Ictaluridae, were unsuitable hosts for0 wzicolov (Table 5).

84 W. R. HAAG AN D M . L . WARREN [Volume 22

TABLE 3. Results of host trials for Lam@is owant~. Letters A to D represent replicate trials using glochidiafrom 4 different female mussels. Sample size (M) is either the number of fish that produced juvenile mussels,or the number of fish that rejected all glochidia and produced no juvenile mussels. + = all fish died beforecompletion of the trial. na = not applicable.

Fishes’



A B C D A B C D

Host

3 (3)39-57s

2 (3)54*

12 (4)42-81

6 (4)39-94

na (0) na (0) na (0) na (0)

1 Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not producejuvenile mussels: Esox nmrricanus (1, 1,2), Cunfpostomn olipkpk (2,2,2), Cyprinelln wwitn (2, 3, 2), Notcmigonuscr~ysokeucns (2,3, 2), Notvopis nmmopl~ihs (2, 3,2), Pimephak~s notatus (2, 3, 2), Zctiobus bubalus (1, 2, 2), Ictaluvus pm-tntus (2, 2, 2), Ambloplitrs ariommus (1, 2, 2-l 4), Lepomis cyu~zcllus (3, 1.6, 2-14), L. mncrockirus (4, 3, 2-22), L. me-g&is (4,3.3, 2%15), Etheostomn rq~estrc (2,3, 2), Pcrcinn nigrof~scinta (2,2, 2)

TABII 4. Results of host trials for Mcdionidus wrl~issi~ws. Letters A and B represent replicate trials usingglochidia from 2 different female mussels. Sample size (M) is either the number of fish that produced juvenilemussels, or the number of fish that rejected all glochidia and produced no juvenile mussels. * = all fish diedbefore completion of the trial. - = the fish species was not used in the trial. na = not applicable.

Fishes’

Mean no. juveniles/fish (M)

Days to transformation Days to rejection (n)

A B A B

HostsAmmocrypta benni 13 (2)

28-51

4 (2)32-38"

3 (2)32-34*

2 (5)32-45

19(l)32-51

20 (1)3842

9 (3)2 5 4 5

36(l)38--65

0 (4)25*

0 (3)35*

2 (2)52-

2 (5)3 1 ”-

na (0)

na (0)

na (0)

na (0)

na (0)

na (0)

na (0)

na (0)

na (0)

-

na (0)

nil (0)

na (0)

-

Marginal hostsEtlreostonln rqcstre 2 (1) 0 (1) 7 (2) 4 (2)

25-38 31%

’ Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not producejuvenile mussels: C,qrt%lln wwtn (7, 4, 2%4), Noteirri~qonlrs cr!/sokwcas (1, 2, 4), Ictnlrrrus punctnt~ts (1, 4, 4), Z~rpomiscy~7cllfrs (2, 1, 4-7), L. nrncrochirus (2, 2, 4-1 l), L. mqp,mlotis (2, 1, 4-ll), Microptrrus snlmoidcs (1, 3, 7)


TABIX 5. Results of host trials for Obouaria unicolor Letters A to D represent replicate trials using glochidiafrom 4 different female mussels. Sample size (n) is either the number of fish that produced juvenile mussels,or the number of fish that rejected all glochidia and produced no juvenile mussels. * = all fish died beforecompletion of the trial. - = the fish species was not used in the trial. na = not applicable.



Fishes’ A B C D A R C D

HostsAmnmcrypta beani - 2 (3) 3 (6) - - na (0) na (0)

21-53* zo-24*

A. meridiana - - 2 (3) 0 (5) - na (0) na (0)21-37” 11*

E~lmstotruz artesim 3 (2) lO(3) 3(l) - na (0) na (0) na (0) -

18-22 2141 18-26

Marginal hostsEtkeostonza nigrum - 0 (25)+ 0 (0) - - na (0) 11 (1)

E. szunini - 0 UN 0;:) l(l) - 60) 11 (2) 11 (1)

0”;0,na 24

I? n&w$asciata 1 (1) 8 (1) 2 (1) 11-19 (6) 6-14 (3) 9-11 (3) 11-18 (7)22 26-28 24

I! sciera 0 (0) ry1, 0 (0) - 19-22 (3) 23 (1) 11 (1) -

n a 23 n a

’ Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not producejuvenile mussels: Esox americanus (1, 1,4), Campostoma oligoolepis (2,3,2), Cyprinclla venusta (2, 3,2), Luxihs ckr,y-socepkalus (2,2.5, 2), Notenzi~o~us crysohcas (1, 3, 2), Notropis amnzopkihs (3,4,2-5), N. atkerinoides (1, 2, 2), N.stilbius (2,2, &5), N. texanus (1,2,2), N. w12~cel21~s (I, 2,2), Pirrqhales fwtntus (2,4.5,2), I? vigilnx (1, 1,2), lctiobusbubahs (1, 3, 2), Anzeiums natalis (1, 1, 2), Ictahrus punctatus (2, 7.5, 2), Noturus Iephxantkus (1, 2, 2), Lepomis cy-anelkrs (1, 2, ll), L. macrockirus (3, 2.6,2-ll), L. nwgaloa2otis (3,2.6, 2-ll), Microptrrus sahoides (3,2.6, 6-ll), Etkeos-tom caerulem (1, 1,2), E. ruf/ineaatunz (1 , 2 , 2), E . rupestre (3,3.3, 2-6), E . stipneum (4, 2 .7 , 2-l I), Per&a katkae(2,1.5,2), l? vigil (1,1,2)

Pleurobema decisum

Plcurobcma decisum is a short-term brooderand was gravid from late spring to early sum-mer. We observed gravid females from 28 Mayto 28 July and found mature glochidia from 8June to 28 July. In the laboratory, both immatureand mature glochidia were released in well-formed conglutinates similar in structure, butdifferent in shape, to those described for E c e r ina(Fig. 2). Conglutinate color varied among, butnot within, individuals and was either orangeor white . In the f ie ld, we observed gravid femaleP decisum releasing conglutinates in a mannersimilar to E cerina and commonly observeddrifting conglutinates in the water column. Inthe f ie ld , we observed schools of b lacktai l shin-ers, Cyprinella venusta, interacting with conglu-tinates as described for E cerina. In the labora-tory, we presented conglutinates to minnows

(Campostoma oligolepis, Cyprinella venusta, Luxilusckrysocepkalus, Lytkrurus bellus, Nocomis lepto-cepkalus, Nofropis atkerinoides, and N. baileyi), anddarters (Percina scicra). All fish species respond-ed to the presence of conglutinates by repeat-edly approaching them closely, but we could notascertain whether f ishes ingested conglutinates .

Glochidia of I! decisum transformed consis-tent ly only on C. venus fa (Cyprinidae) (Table 6)and inconsistently on an additional minnowspecies , L. ckrysocepkalus. Fourteen minnow spe-cies were unsuitable hosts. Nine other fish spe-cies , representing the famil ies Centrarchidae, Ic-taluridae, and Percidae, were unsuitable hostsfor P decisum (Table 6).

Quadrula asperata

Quadrula asperata is a short-term brooder andwas gravid from spring to early summer. We

86 W . R . HAAG A N D M. L . WARREN [Volume 22

TAKE 6. Results of host trials for PI~fr~~~bc~na dccisurr~ Letters A to D represent replicate trials using glochidiafrom 3 different female mussels. Sample size (I?) is either the number of fish that produced juvenile mussels,or the number of fish that rejected all glochidia and produced no juvenile mussels. * = all fish died beforecompletion of the trial. - = the fish species was not used in the trial. na = not applicable.


Days to transformation Days to rejection (M)

Fishes’ A R C D A B C D

HostsClJprimG7 Lwl~sta 2 (3) 2 (10) 0 (5) 2 (5) na (0) na (0) na (0) na (0)

24 16-22 5” 23-37

Marginal hostsLfuilzrs chrysocrphnlus 0 (3) 0 (0) 2 (5) 1 (1) na (0) 2-13 (4) na (0) 10 (2)

23” na 17-21 1 7

I Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not producejuvenile mussels: Canzposto~~a oli~dcpis (3, 3.6, 2-Y), Cyprine2ln callistin (4, 2.2, 2-17), Hybopsis -windrelli (1, 1, 2),L~ythrms bellus (4, 3, 2-6), Noco~ms kptocephnlus (3, 3.6, 2-lo), Notr~nigorms cry~oImzns (3, 3.6, 2-E), Notropis am-nq~l~ilu~ (2,3.5,2-3), N. nthrrinoides (3,2.3,2-3), N. boil+ (3,3,2-3), N. stilbius (3, 3.6,2-3), N. tcramrs (3,2, 2-3),N. zducchs (3,3,2-3), Pimphales mtntus (3,1.6,2-3), I! vigilnx (1, 1,2), Noturus leptncnnthus (1,2,2), Lrpomisc~yne~hs (1, 3, 6), I.. rrfacrochirus (1, 2,2), I.. mega:nlotis (2, 1.5,2), Micropterus sn2nzoides (2, 3.5,2-15), Ethmstonznavksiar (2,2.5, 2-15), E. rupestw (2,4.5, 2), Pncim r?igrojascintn (1, 1,3), I? sckrn (1, 2,2)

observed gravid females from 17 April to 28 July ture glochidia, and many glochidia were boundand found mature glochidia from 17 June to 28 in this mucus. In dissected individuals, mucusJuly. In the laboratory, mature glochidia were re- was also associated with glochidia inside theleased freely and were not contained in conglu- gills. Long strands of mucus often issued fromtinates. Copious mucus was released with ma- the excurrent siphon of releasing females, simi-

TARLX 7. Results of host trials for Quadrula asperntn. Letters A to C represent replicate trials using glochidiafrom 3 different female mussels. Sample size (n) is either the number of fish that produced juvenile mussels,or the number of fish that rejected all glochidia and produced no juvenile mussels. + = all fish died beforecompletion of the trial. - = the fish species was not used in the trial. na = not applicable.

Mean no. juveniles/fish (M)

Fishes’

Days to transformation Days to rejection (~7)

A B C A B C

Hostslctnlflrlrs pllilctntlrs

Marginal hostsNoturus kptacnntlm

4 (6)25-27

0 (0)na

o* (3)22*

0 (0)nn

2 (5)17-34

1 (1)3 1

na (0)

3 (2)

na (0)

2 (2)

na (0)

26 (1)

’ Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not producejuvenile mussels: Cnmpostofm oligolcpis (1, 4, 3), C!yprinclln cnllistin (1,2,3), C. cI1IpxIrfl (I, 3,2), C. zw~~tste (3,3.3,2-6), I.milus clrrysocq~hnlus (I, 4, 3), Lythrums bellus (1, 2, 3), Noconris lq~tocq~lzn/~~s (1, 2, 3), Notew~~gor71rs cr!ysoleucns(3, 3, 2-7), Notmpis nmmpl~ib~s (1, 4, 3), N. ntlrminoidc~s (2, 2.5, 2-3), N. bnikyi (2, 2.5, 2-6), N. stdbius (1, 1, 3), N.tcxnmfs (1, 2, 3), N. solrrccll~~s (2, 2.5, 2-3), Pinq~llc?les &nt~rs (1, 4, 3), Ictiobm b~rbnlus (2, 3.5, 2-6), Moxostonm poe-cilurum (1, 1, 3), Rmciwm rmtnlis (2, 2.5, 4-18), Fund~rlus olizmceus (1, 1, 18), Lqwmis cyla,z~lhrs (2, 2, 3-4), L. mam-chirus (2, 2, Z-3), L. vqwlotis (3, 2, 2-4), Microptcws solmides (3, 2.6, 2-4), Pomoxis mmrlnris (1, 2, 3), Annmmyptomrridima (1, 2, 4), Etlmslom rqmtrr~ (2, 3.5, 2-6), Pmim nigrOJmintn (2, 2.5, 3-4), )? scim (1, 2, 3-6)

20031 MUSSEL HOSTS AND INFECTION Sl’RA1‘EC1ES 87

lar to Elliptio I~I’CII. Immature glochidia and eggswere re leased in i rregular c lusters , as descr ibedfor E. nrca.

Glochidia of Q. aspmta transformed consis-tently on channel catfish, lcfolurcrs punctafus (Ic-taluridae) (Table 7). One additional catfish spe-cies, Notlrrus kptacanthrs, was a marginal host.One catfish species, Anwiz~rus Iiatnlis, was an un-suitable host. Twenty-seven other fish species,representing the families Catostomidae, Cypri-nidae, Centrarchidae, Fundulidae, and Percidae,were unsuitable hosts for Q. asprmta (Table 7).

Discussion

All 7 mussel species in our study were hostspecialists, with host use restricted to a singlefamily or genus of f i shes . Host use for most spe-cies was concordant with host information ob-tained by laboratory infection trials for closelyrelated species. For example, primary host useof Ellipfio dilatata is limited to darters and scul-

pins (Luo 1993), similar to E. nrcn, which usesonly darters ; sculpins do not occur in the S ipseyand Buttahatchee rivers (Boschung 1989). Hostsfor Fusconaia COY and F C~AMPO~~S include a widevariety of minnows (Neves 1991, Bruendcrmanand Neves 1993, respectively), and are similarto F: ccrina. Host use of MPdimidm cmrndicus, M.pmicillatus, and a small-stream populat ion of M.acutissinnrs is restricted to darters (Zale and Ne-ves 1982, O’Brien and Williams 2002, and Haagand Warren 1997, respect ively) and is s imilar tolarge-stream populat ions of M. acufissirmrs. Hostuse of hmpsi/is or&n is restricted to Micropferlrsspp., similar to a large number of other speciesof Lampsilis (reviewed in Haag et al. 1999). Hostuse of P/cmhwrn decision is similar to 7 otherspecies of IJk’1~rohCJJJ17 (I? ch7, I? COCCiJlCUJJ1, I? col-

/Iran, I? cordatnm, f?flfilrzflrrJl, I! OIJ@‘JJ~C~, and I! p/r-iformc), for which host use is restricted mostlyto minnows (C)‘Dee and Watters 2000, Hove etal. 1997, Hove and Neves 1994, Yokcly 1972,Haag and Warren 1997, Weaver et al. ‘1991,O’Brien and Williams 2002, respectively). Hostinformat ion based on laboratory t r ia ls for c loserelatives of Qzradrh nsywnfn is available only forQ. ~robilis and Q. pfrshrkxa, for which host use issimilar (catfishes: Howclls 1997, Coker et al.1921, respectively). The similarity of host LISA

among congeneric mussel species indicates that

th is t ra i t i s h ighly conserved at lower taxonomiclevels and may be highly predictable amongclosely re lated mussel species .

Apparent departures from patterns of hostuse among ostensibly closely related musselspecies may ref lect incomplete understanding ofphylogenet ic re lat ionships within these groups.Host use of Qundrda cy/iJdricn and Q. ir?l?rrrJnlinis restricted to 3 minnow genera (Yeager andNeves 1986, Yeager and Saylor 1995, respective-ly), departing widely from host-use patterns ofother species of Quadrlrh. However, recent workshowed that these 2 species are members of amonophyletic &de distinct from other mem-bers of the genus (Serb et al. 2003). Similarly,host use of ~~rsco~raia ~br1117 (restricted to skipjackherring, Ahtl chrysoclhris, Cokcr et al. 1921)differs from other species of FJnscorJaitl but, ascurrent ly recognized, this genus is polyphylet icand E r+rrzn is not closely related to other mem-bers of the genus (Lydeard et al. 2000). Elliptic>is a large genus with most species occurring incoastal streams on the Atlantic slope or easternGulf of Mexico (Davis et al. 1981); species fromthese drainages use sunfishes (Centrarchidae)or yellow perch (Pica ~7clirsc~1s) as hosts (E.comp/aru?fa, Matteson 1948; E. buckkyi and E. ic-krina, Keller and Rues&r 1997), in contrast toE. NT~I and E. dilntafa from interior streams inthe Mobi le and Mississ ippi basins , respect ively .Differences in host use between these speciesgroups provide evidence for divergent phylo-genetic lines within Elliptic.

Other apparent departures from well-estab-l ished phylogenet ic patterns of host use are l ike-ly a result of differences in host-identificationmethods among studies. Many host relation-ships reported in the early l i terature were basedon observat ions of natural infestat ions only andwere not confirmed by laboratory transforma-tion experiments . Most glochidia at tach readi lyto nonhost- f ish species but are later re jected, sosuch observat ions potent ia l ly resul t in erroneoushost relationships. Furthermore, in some casts,these relationships are based on probable mis-identifications of encysted glochidia (see ac-count for E!/ipfio crassidcrJs in Brim Box and Wil-liams 2000). Host information based on a widevariety of methods has been summarized inseveral reviews (Fuller 1974, Hoggarth 1992,Watters 1994) . Despite cautionary statements bythese authors, circumstantial or potentially er-roneous host re lat ionships reported in these re-

88 W. R. HAAG AND M. L. WARREN [Volume 22

views have been widely and uncritically cited(e.g., Parmalee and Bogan 1998). We stress theneed to critically examine original sources ofhost information and methods of study beforemaking and report ing conclusions about musselhost use.

Host-attraction strategies

The mussel species in this study used a di-verse array of s t ra tegies for infect ing host f i sheswith glochidia. Two previously described hoststrategies, lure-displaying host-specialists andconglutinate-producing host-specialists (Haagand Warren 1998), are represented in this groupof species but, for 3 species, the method of hostinfect ion was unclear .

Lure-displaying host-specialists were repre-sented by Medionidus acutissimus and Larnpsilisornata. In this strategy, gravid females displaylures that elicit attacks from host fishes, result-ing in host infection (Haag and Warren 1999).Lures of this type have been described for sev-eral other species of Lampsilis (Kraemer 1970,Barnhart and Roberts 1997, Haag et al. 1999).Modified mantles similar to those describedhere for M. acutissiml*s have been reported forM. pmicillatus (Brim Box and Williams 2000),and similar displays in the wild have been ob-served for M. conradius (S. Ahlstedt, US Geo-logical Survey, Knoxville, Tennessee, personalcommunicat ion) . In Lafnpsilis, large mantle luresse lec t ive ly target sui table host f i shes by mimick-ing prey items of these fishes, reducing theprobabi l i ty of infect ion of unsui table f i sh species(Haag and Warren 2000). The modified mantleof Medionidus likely has a similar function, al-though interactions with fishes have not beenobserved. Because of the small size of the lureand the location of displaying females withinthe interst ices of coarse substrates , the lure maybe inconspicuous to most fishes except darters(the sole host for Mediorlidus), many species ofwhich typically feed among gravel and cobblesubstrates (Page 1983).

Conglut inate-producing host -specia l is ts wererepresented by Fuscormia cerina and Pleurobel~ln&C~SUI?I. In this s trategy, females re lease glochid-ia in small packets, which resemble food itemsof small, predaceous fishes such as darters andminnows. This strategy is known for severalother species of F~sconnin and PI~urobcnzn(Bruenderman and Neves 1993, Hove and Neves

1994, Haag and Warren 1997). It is hypothesizedthat this strategy facilitates host infectionthrough the ingest ion of conglut inates by smal lfishes, but observations of conglutinate releaseand interactions with fishes in the wild are rare(but see Jones et al. 1986). In the laboratory, weobserved a large number of f ish species , includ-ing many unsuitable hosts, feeding on or oth-erwise interacting with conglutinates in waysthat could result in glochidial transmission. Incontrast, in the field, we observed interactionsof conglutinates of both mussel species onlywith the blacktail shiner, Cyprinella venusta, aprimary host for both species. Cyprinella zwustaoccurs most commonly in the mid-water col-umn in moderate to swift riffles (Baker andRoss 1981), and most food i tems are taken fromthe drift (Ross 2001). Based on the prevalence ofinfestations of wild fishes, Bruenderman andNeves (1993) hypothesized that drift-feedingminnows were the primary hosts of E cunenlusand I! ouifornw in Virginia. The conglutinate-re-lease behavior we observed for E cerina and I!deciswn resulted in conglutinates being sus-pended in the mid-water column where theywere vulnerable to C. venusta and other drift-feeding minnows, but less vulnerable to unsuit -able hosts such as darters and other benthic-feeding f ishes.

Elliptio arca and Quadrula asperata displayedno modified mantle lures and did not releasemature glochidia in conglutinates. During han-dling, both species, as well as other short-termbrooders (Yeager and Neves 1986), often abortimmature g lochidia or eggs in s t ructures resem-bling conglutinates, but this behavior does notrepresent a strategy for host attraction. Rather,transmiss ion of g lochidia to hosts may be fac i l -itated by entanglement of fishes in mucousthreads, which are released in association withand contain mature glochidia. Release of mucusor other web- l ike s t ructures in assoc iat ion withglochidia has been observed in host-specialists(Matteson 1948, Yokely 1972, Woody and Hol-land-Bartels 1993) and host-general ists (Lefevreand Curtis 1910, Wood 1974, Haag and Warren1997). Such a strategy would be effective forgeneral is ts because a wide variety of f ishes l ike-ly would be infected indiscr iminately . For host-specialists, such a strategy seems maladaptivebecause the likelihood of infection of nonhostfishes and subsequent loss of these offspringwould be high. Our observations of glochidial


release by E. arca and Q. asyernta were madeonly in the laboratory and may not be represen-tat ive of re lease behaviors in the wild. Fie ld ob-servations are needed to ful ly elucidate host-at-traction strategies for these species.

We made no observat ions of Obovaria unicolorin the field or laboratory that suggested poten-tial host-attraction strategies for this species.Animals did not display mantle lures, did notproduce conglutinates, and did not release mu-cus in association with glochidia. Glochidiawere brooded only in the posterior portion ofthe outer gills and were not associated with mu-cus or any conglutinate structure. These brood-ing traits are shared with the genera Epioblasma,Medionidus, Lampsilk, Ligumia, Toxolama, andVillosa, all of which display lures. It is thereforepossible that 0. unicolor possesses a lure that wedid not observe. However, in lure-displayingspecies , modif ied mantle margins that composethe lures are visible even when the lure is notdisplayed (Haag et al. 1999); such a structurewas not evident in 0. unicolor. Obovaria unicolorwas found in close association with its primaryfish host; both 0. unicolor and sand darters (Am-mocrypta spp.) occur most f requent ly in c lean orsilty sand in low-flow areas (Ross 2001, WRHand MLW, unpublished data). Sand darters feedmostly on midge larvae (Diptera), but also in-gest other small prey, including larval Asianclams (Covbicula,f7uminea) (Ross 2001). Glochidiabroadcast in this habitat may have a high like-lihood of being encountered and ingested byforaging sand darters. However, no NorthAmerican mussel species are currently knownto broadcast glochidia and rely on passive in-fection of host fishes; rather, all well-studiedspecies exhibit some type of strategy to facilitatehost infection. Further field and laboratory ob-servations are needed to determine the host-in-fect ion mode for this species .

ltq~lications for conservatio~7

Mussel populat ions in the Mobile Basin, as inmost of North America, have declined over thelast 30 y (Neves et al. 1997). In some rivers, de-clines in mussel populations are attributed todisappearance or declines of host fishes, result-ing in reduced mussel reproductive success(Smith 1985, Khym and Layzer 2000). Thismechanism is insuff ic ient to explain decl ines ofthe 7 mussel species in this study because all

species use common, widespread fishes ashosts. Pleurobema decisurn, a federally endan-gered species, consistently used only one fishspecies, Cyprinella venusta, as host. Although insome cases, use of only one fish species may beconsidered a conservat ion l iabi l i ty , C. venusta i sone of the most widespread and abundant fish-es in the western Mobile Basin (Boschung 1989,Ross 2001). Furthermore, C. venusta is tolerantof highly degraded habitats including impound-ed and channelized streams (Mettee et al. 1996,Ross 2001). Medionidus acutissimus, a federallythreatened species, uses many darter species ashosts, including abundant and widespread spe-cies such as Percina nigrofasciata. Obovaria unicolorhas experienced a dramatic recent decl ine in theButtahatchee River (Hartfield and Jones 1990,Jones 1991). We have no data on current popu-lation levels of sand darters and Etheostoma ar-tesiae (hosts for 0. unicolor) in the ButtahatcheeRiver , but these f ishes are currently widespreadand common in other t r ibutar ies of the Tombig-bee River in Alabama and Mississippi (Metteeet al. 1996, Ross 2001, MLW and WRH, unpub-lished data). Clearly, factors other than loss off ish hosts (e .g . , a l tered f lows, habitat loss , water-qual i ty degradat ion) are responsible for decl inesof these and other freshwater mussels in theMobile Basin.

Acknowledgements

We thank J. G. McWhirter, A. Greer, J. L. Sta-ton, T. Fletcher, T. Slack, T. Mann, I? Hartfield,A. Sheldon, J. Layzer, C. Lydeard, D. Carlson,C. Jenkins, and E McEwen for the i r var ious con-tributions to this study. This study was sup-ported by the Mississippi Wildlife HeritageFund and the Southern Research Station, US De-partment of Agricul ture , Forest Service .

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