Host fishes and infection strategies of freshwater mussels in large Mobile 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, 38655 LISA

Abstract. We investigated host fishes, timing and modes of glochidial release, and host-attraction strategies for 7 of freshwater mussels from the Buttahatchee and Sipsey rivers (Mobile Basin), and Mississippi, USA. We determined hosts as fish species that produced juvenile mussels from laboratory-induced glochidial infections. We established the following primary mussel/host relationships: Elliytio nrcn with Etl~~~tomu nrtcsinc and Percitza ~zigr#scintu; Fusconain cerina with 6 species of minnows (Cyprinidae); Lm7psilis ormtn with Micropkrus sahoidcs; Mcdionidus acutissimus with 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-attraction strategies that targeted their specific host fish. Fusronnin cerirla and I! dmisurn released glochidia in conglutinates that elicited feeding responses from fishes in the field and in the laboratory. Gravid female Dmrpsilis ornatn and M. ncutissimus displayed mantle lures. Host-attraction strategies were less apparent for E. arcn and (2. nspmdn, but these species released glochidia in association with copious mucous secretions, which may serve to entangle fishes, facilitating host infection. No host-attraction strategy was apparent for 0. uiiicolor. Kr?/ zards: host-parasite relationship, life history, Unionidac, , mussels, glochidia, Mobile Basin.

The southeastern United States supports the ican mussel species. This lack of knowledge most diverse freshwater mussel fauna on earth. hampers conservation efforts and limits our un- This fauna also is distinguished as one of the derstanding of the ecology of these . most endangered groups of organisms in North The Mobile Basin of Alabama, Georgia, Mis- America (Neves et al. lYY7). The basic life his- sissippi, and Tennessee is home to a unique, tories of many southeastern mussel species are highly endangered mussel fauna including a poorly known. To complete development, larvae large number of endemic species (Stansbery (glochidia) of most mussel species must under- 1976, Lydeard and Mayden 1995). The Butta- go a brief period as ectoparasites on the gills or hatchee and Sipsey rivers support the best re- fins of fishes. Host specificity ranges from gen- maining examples of large-stream Mobile Basin eralists, able to parasitize a wide variety of fish- mussel communities. Host information exists for es, to specialists, whose glochidia can develop a number of headwater species in the Mobile on only a few, usually closely related fish spe- Basin (Haag and Warren 1997, Haag et al. 1999), cies (Haag and Warren 1997). Larvae cncounter- but hosts are unknown for most large-stream ing an unsuitable host are rejected by the fish species in the basin. immune system (O’Connell and Neves 1099). We investigated host fishes, timing and Many species display remarkable adaptations to modes of glochidial release, and host-attraction facilitate transmission of glochidia to hosts, in- strategies for 7 species of mussels from the But- cluding display of lures and release of glochidia tahatchce and Sipsey rivers: Alabama spike (EI- in packets that mimic food items of host fishes liptio nrcn), Gulf pigtoc (Fuscouaia cerina), south- (e.g., Barnhart and Roberts 1997, Haag and War- ren lYYY, Watters 1999, Jones and Neves 2002). ern pocketbook (Laqwilis orunto), Alabama Knowledge of host fishes, host-attraction strat- mot casinshell (MeJiorlidus achssimus), Alabama egies, an d other aspects of reproductive biology hickorynut (Obtn~~7rin frrricoh), southern club- sheii (I’lrlrlobc~~rn dccimm), and Alabama orb is lacking or incomplete for many North Amer- (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 occurs of each individual by gently prying apart the in the Amite, Pearl, and Pascagoula rivers (Wil- valves and examining the gills. We recognized liams and Fradkin 3 999), and L. ornntn is endem- gravid females by the presence of distended ic to Gulf of Mexico drainages from the Amite gills. We immediately returned male and non- River east to the Escambia River (Williams and gravid specimens to the stream. We brought Butler 1994). The US Fish and Wildlife Service gravid mussels into the laboratory and placed recognizes I? &cist~~~ and M. acutissimus as en- them into individual, aerated beakers at room dangered and threatened, respectively. The temperature (21-25°C). Most individuals of E. American Fisheries Society considers E. nrcn urea, E ccrinn, I! decisum, and Q. nsperata released threatened, and L. ornatn, 0. unicolor, and Q. as- glochidia into the beakers within 24 to 48 h; we per&a species of special concern (Williams et al. used these glochidia in host trials immediately 1993). Along with 2 other species not studied upon release. Lnmpsilis orrlntn, M. acutissimus, here (Q&rula rumphinna and Tritogonia uerru- and 0. u~zicolor did not release glochidia in the cclsa), these 7 species dominate mussel commu- laboratory. With the exception of P deciszrl~z and nities in the Buttahatchee and Sipsey rivers M. acutissimxs, we harvested glochidia from in- (WRH and MLW, unpublished data). dividuals that did not release in the laboratory by sacrificing the and dissecting the Methods gills. WC harvested glochidia from M. ncutissi- rnzls by flushing the contents of the gills into a We determined host fishes by inducing glo- beaker using a hypodermic syringe and aged chidial infestations in laboratory trials and mon- tap water. Because of their federal conservation itoring the rejection of glochidia or production status, M. aczrtissimus and l? decisum were re- of juvenile mussels. Our methods were de- leased alive where they were collected within 7 scribed by Haag and Warren (1997) and are d of collection. We worked with these 2 species based on a standard host-identification protocol under US Fish and Wildlife Service Endangered (Zale and Neves 1982). We identified primary Species Subpermitee Authorization Number SA- host-fish species as those that consistently pro- 98-06, Mississippi Department of Wildlife, Fish- duced live juvenile mussels. We identified un- eries, and Parks Scientific Collecting Permit, and suitable host-fish species as those in which all Alabama Department of Conservation Scientific mussel glochidia were rejected from all individ- Collecting Permit Number 182. ual fishes without producing juvenile mussels. We based descriptions of gravid periods on a In some cases, some individuals of a particular composite of field observations from 3 996, 1998, fish species rejected all glochidia, but others 2000, and 2001; we based descriptions of host- produced juvenile mussels. Because of inconsis- attraction strategies and glochidial release on tent glochidial transformation, we regarded field and laboratory observations from the same these fish species as marginal hosts. For cac11 period. We classified species into 1 of 2 catego- mussel species, we ran 2 to 4 replicate trials (20- ries, short-term or long-term brooders, based on 22”C), using glochidia from a different female in the duration and timing of the gravid period each trial. We exposed glochidia from each mus- (Kat 1984). We used glochidia from gravid fe- sel species to 15 to 34 fish species (l-10 individ- male mussels from the following localities and uals of each). We chose fish species to represent dates in host-identification trials (trials are iden- most families and genera and all common spe- tified as A, B, C, or D): Alabama-Sipsey River, cies present at study sites (Boschung 1989). Pickens-Greene Co.: E. arca, A, 6 July 1998, B, 27 We collected gravid female mussels from the June 2001; E crrirza, A, 10 June 1998, B, 8 July Buttahatchee River, Monroe Co., Mississippi 1998, C, 29 July 1998; L. orrznfa, A and B, 6 July and the Sipsey River, Pickens/Greene Co., Ala- 1998; 0. urzicolor, A, 17 June 1998, B, 26 June bama in June and J~tly 1998 and 2001. Both 1998, C and D, 27 June 2001; I! ciecis44n4, A, 14 streams are large tributaries of the Tombigbee July 1998, B, 29 July 1998, D, 3 July 2001; Q. River (Mobile Basin). Water temperature at the nsprrntn, A, 26 June 1998, B, 14 July 1998; Mis- time of collection was 22 to 30°C. We collected sissippi-Buttahatchee River, Monroe Co.: E mussels by diving and, in shallow areas, by ccrina, D, 22 June 2001; L. orllata, C and D, 28 searching the stream bottom using a glass-bot- June 2001; M. acutissimus, A, 21 June 2001, B, 28 tomed bucket. We assessed reproductive status June 2001; (2. ilspcrata, C, 22 June 2001. We de- 80 W. R. HAAG AND M. L. WAMEN [Volurne 22

TAMI.I: 1. Results of host trials for Elliptic RITZ. Letters A and I3 rcpresent replicate trials using glochidia from 2 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. - = the fish species was not used in the trial. na = not applicable.

Mean no. juveniles/fish (II)

Days to transformation Days to rejection (n)

Fishes’ A B A B Hosts 8 (3) 9 (3) na (0) na (0) 19-29 22-35 5 (2) - na (0) - 15-19

- 3 (1) - 4 (1) 33

’ Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not produce jUVellih2 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 the earthworms and minnows (sunfishes), and pel- Mississippi Museum of Natural Science letized fish food (channel catfish). (MMNS), Jackson, Mississippi and the Illinois Natural History Survey, Champaign, Illinois. Results We collected most potential host fishes from the following streams in the western Mobile Ba- Elliptio arca sin: Alabama-Clear Creek (Black Warrior Riv- er system), Winston Co.; Mississippi-Bull Ellipfio ~IYCIZ is a short-term brooder and was Mountain Creek (Tombigbee River system), Ita- gravid from late spring to early summer. We ob- wamba Co.; Noxubee River (Tombigbee River served gravid female E. arca from 28 May to 28 system), Winston Co.; Hashaqua Creek (Tom- July and mature glochidia from 27 June to 28 bigbee River system), Noxubee Co. We aug- July. In the laboratory, mature glochidia were re- mented fish collections with specimens from the leased freely and were not contained in conglu- following streams: Alabama-Cedar Creek tinates. Some glochidia were released in small (Tennesee River system), Franklin Co.; Missis- clusters that disassociated quickly after release. sippi-Goodwin Creek (Yazoo River system), Copious mucus was released with mature glo- Panola Co.; Lee Creek (Yazoo River system), La- chidia, and many glochidia were bound in this fayette Co.; and Little Tallahatchie River (Yazoo mucus. Long strands of mucus often issued River system), Lafayette Co. We collected all from the excurrent siphon of releasing females. fishes from stream sites without mussels or Immature glochidia and eggs were released in with low mussel densities to avoid using fish irregular clusters, which conformed loosely to with pre-existing glochidial infestations or ac- the shape of the gill water tubes. These clusters quired immunity to glochidia (Zale and Neves resembled true conglutinates (see E cuina) but 1982). We obtained Ictnlnrus punctatus, Micrcp lacked a regular, cohesive shape, and never con- terrrs snln~)i&s, and Notmzi~mus crysolcuc~zs from tained mature glochidia. hatchery stock. We maintained all fishes in aer- Glochidia of E. arca transformed consistently ated aquaria in the laboratory and fed them on only 2 darter species (Percidae): Efhcosfomn bloodworms (minnows, darters, madtoms), nrfrsiae and krcinrr nigrqfiwiofa (Table 1). Glo-

82 W. R. HAAG AND M. L. WARIXEN [Volume 22 schools of blacktail shiners, Cyprinella venusta, unsuitable hosts. Ten other fish species, repre- repeatedly approaching drifting conglutinates. senting the families Catostomidae, Cyprinidae, Because of the fishes’ rapid movements, we Esocidae, Ictaluridae, and Percidae, were unsuit- could not discern whether shiners ingested con- able hosts for L. ornata (Table 3). glutinates; in most cases, the fishes approached conglutinates very closely and then veered off acutissimus just before, or at, the moment of contact. If shin- ers did ingest conglutinates, contact was brief, Medionidus acufissinzus is a long-term brooder and conglutinates were expelled quickly. In the and was gravid from approximately October to laboratory, we presented conglutinates to min- June of the following year. By late May, gills of nows (C. vemsta, Nocolnis leptocepkulus, and No- most females had only 2 to 3 gravid water tubes fropis ammopkilus), darters (Etkeostoma rupestrc (fully charged gills have -3040 gravid water and Percina sciera), and sunfish (Lepomis macro- tubes). Most females were spent from early JUne ckirus). All fish species responded to the pres- to October. Females did not release glochidia in ence of conglutinates by repeatedly approaching the laboratory. We observed several gravid fe- them closely as observed in the field, but again, males in the Sipsey and Buttahatchee rivers dis- in most cases, we could not discern if individ- playing small, black modified mantle margins. uals ingested conglutinates. We observed an in- When displaying, females were widely agape dividual of E. rupestre ingest and expel a con- and completely unburied but were often lying glutinate 3 times in rapid succession. within the interstices of coarse gravel or cobble Glochidia of E cerina transformed on a wide substrates in swift currents. Females usually variety of minnow species (Cyprinidae) (Table were tethered to a pebble by a byssal thread. 2). Glochidia transformed consistently on 6 min- We observed displaying individuals in a variety now species and inconsistently on 6 additional of orientations with the dorsal margin facing up, minnow species. Five minnow species were un- the ventral margin facing up, or lying on their suitable hosts. Fourteen other fish species, rep- side. The modified portion of the mantle ex- resenting the families Catostomidae, Centrar- tended along the ventral margin of the shell chidae, Ictaluridae, and Percidae, were unsuit- from the posterior tip to slightly anterior of the able hosts for E cerina (Table 2). midpoint of the shell. The modified mantle was matte, inky black with a small (-2 mm2), white Lampsilis ornata patch located at about the midpoint of the shell, near the anterior-most portion of the modified Lampsilis ornata is a long-term brooder and mantle margin. The white patch flickered rap- was gravid from late summer to late spring of idly at -1 s intervals; the motion was similar to the following year. We found gravid individuals the flickering of a television screen. With the ex- throughout most of the year with the exception ception of the flickering mantle patch, display- of July to September when most females were ing females appeared moribund and showed lit- spent. Lampsilis ornata did not release glochidia tle response to handling. Females remained in the laboratory. Gravid females displayed a widely agape when removed from the water, large mantle lure that we observed in the labo- and did not attempt to close the shell or retract ratory and in the field. The lure consisted of a the mantle margins. The flickering motion of the pair of elongated flaps e-50 to 75 mm long, white patch often continued for 15 s or more which protruded beyond the shell margin, with after being removed from the water. These be- the gravid gills visible between the flaps. Each haviors were not observed in the laboratory. flap was cream colored with a distinct eyespot Glochidia of M. acutissimus transformed on a and a dark, lateral stripe, and flaps were pul- wide variety of darter species (Percidae) (Table sated vigorously during display. The lure and 4). Glochidia transformed consistently on 8 display behavior closely resembled that de- darter species. Another darter species, E. ruyes- scribed for L. cardiwn (Kraemer 1970, Haag and tre, was a marginal host. No darter species were Warren 1999). identified as unsuitable hosts. Seven fish spe- Glochidia of L. ornata transformed only on cies, representing the families Centrarchidae, largemouth bass, Micro~~trrtrs salmoides (Centrar- Cyprinidae, and Ictaluridae, were unsuitable chidae) (Table 3). Four centrarchid species were hosts for M. acutissirmts (Table 4). 20031 MUSSEL HOSTS AND INFECTION STRATEGIES 83

TAIXT 2. Results of host trials for Fwco~zai~ c&m. Letters A to D represent replicate trials using glochidia from 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 before completion of the trial. - = the fish species was not used in the trial. na = not applicable.

Mean no. juveniles/fish (n)

Days to transformation Days to rejection (II)

Fishes’ A B C D A B C D

- 20) - 6 (4) - na (0) - na (0) 15 24-32 * * 2 (2) 15 (7) 22 (1) na (0) na (0) na (0) - 19-21 19-26 24 - 1 (1) - na (0) 20 * 1 (3) o* (3) 3 (3) na (0) na (0) na (0) 19-21 15 24-31 - - - 2 (3) - na (0) 27-31 * 2 (4) 1 (1) - na (0) na (0) 14-21 18-27

0 (0) 2 (3) 1 (4) * 2 (4) 5-7 (2) 3 (1) L 14-16 18-27 0 (f-3 “Yb) 1* (1) 2 (1) 2-5 (I) 5 (2) na (0) 3 (1) na ‘ 14 18 0 (0) 0;) 4 (3) 1 (2) 2 (2) 2-14 (3) 13 (1) 3 (1) na na 14-19 20-24 - - 7 (1) - 0 (0) - 2 (2) 3 (1) 21 - - 2nF3) - - 3-6 (2) 18-26 - * 0 UN I* (3) - * 2-20 (3) 12 (1) na 14

’ Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not produce juvenile 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 ture glochidia by November. Females did not re- lease glochidia in the laboratory, and we ob- Oboumk zmicokv is a long-term brooder and served no mantle displays in the field or labo- was gravid from approximately August to June ratory. of the following year. Glochidial release took Glochidia of 0. ~nicolou transformed consis- place from April to June. We observed fully tently on 3 darter species (Percidae) and incon- gravid and partially spent females from April sistently on 4 additional darter species (Table 5). to early June. After 8 June, we found only par- Six darter species were unsuitable hosts. Twen- tially spent individuals and, after 26 June, all ty other fish species, representing the families females were completely spent. By late August, Catostomidae, Centrarchidae, Cyprinidae, Eso- we found gravid females that were brooding cidae, and Ictaluridae, were unsuitable hosts for embryos. We observed gravid females with ma- 0 wzicolov (Table 5). 84 W. R. HAAG AND M. L. WARREN [Volume 22

TABLE 3. Results of host trials for Lam@is owant~. Letters A to D represent replicate trials using glochidia from 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 before completion of the trial. na = not applicable.

Mean no. juveniles/fish (n)

Days to transformation Days to rejection (II)

Fishes’ A B C D A B C D

Host 3 (3) 2 (3) 12 (4) 6 (4) na (0) na (0) na (0) na (0) 39-57s 54* 42-81 39-94

1 Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not produce juvenile mussels: Esox nmrricanus (1, 1,2), Cunfpostomn olipkpk (2,2,2), Cyprinelln wwitn (2, 3, 2), Notcmigonus cr~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 using glochidia from 2 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 before completion of the trial. - = the fish species was not used in the trial. na = not applicable.

Mean no. juveniles/fish (M)

Days to transformation Days to rejection (n)

Fishes’ A B A B Hosts Ammocrypta benni 13 (2) 0 (4) na (0) na (0) 28-51 25* 4 (2) na (0) 32-38" - 3 (2) na (0) 32-34* 2 (5) 0 (3) na (0) na (0) 32-45 35* 19(l) 2 (2) na (0) nil (0) 32-51 52 20 (1) - na (0) 3842 9 (3) 2 (5) na (0) na (0) 2545 31” - 36(l) - na (0) 38--65 Marginal hosts Etlreostonln 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 produce juvenile mussels: C,qrt%lln wwtn (7, 4, 2%4), Noteirri~qonlrs cr!/sokwcas (1, 2, 4), Ictnlrrrus punctnt~ts (1, 4, 4), Z~rpomis cy~7cllfrs (2, 1, 4-7), L. nrncrochirus (2, 2, 4-1 l), L. mqp,mlotis (2, 1, 4-ll), Microptrrus snlmoidcs (1, 3, 7) 20031 MUSSEL HOSTS AND INFECTION STRATEGIES 85

TABIX 5. Results of host trials for Obouaria unicolor Letters A to D represent replicate trials using glochidia from 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 before completion of the trial. - = the fish species was not used in the trial. na = not applicable.

Mean no. juveniles/fish (n)

Days to transformation Days to rejection (II)

Fishes’ A B C D A R C D Hosts - - Amnmcrypta 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 hosts - - Etkeostonza nigrum - 0 (25)+ 0 (0) na (0) 11 (1)

E. szunini - 0 UN 0;:) l(l) - 60) 11 (2) 11 (1) na 24 I? n&w$asciata 1 (1) 0”;0, 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) - na 23 na

’ Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not produce juvenile 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), lctiobus bubahs (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 (Campostoma oligolepis, Cyprinella venusta, Luxilus ckrysocepkalus, Lytkrurus bellus, Nocomis lepto- Plcurobcma decisum is a short-term brooder cepkalus, Nofropis atkerinoides, and N. baileyi), and and was gravid from late spring to early sum- darters (Percina scicra). All fish species respond- mer. We observed gravid females from 28 May ed to the presence of conglutinates by repeat- to 28 July and found mature glochidia from 8 edly approaching them closely, but we could not June to 28 July. In the laboratory, both immature ascertain whether fishes ingested conglutinates. and mature glochidia were released in well- Glochidia of I! decisum transformed consis- formed conglutinates similar in structure, but tently only on C. venusfa (Cyprinidae) (Table 6) different in shape, to those described for E cerina and inconsistently on an additional minnow (Fig. 2). Conglutinate color varied among, but species, L. ckrysocepkalus. Fourteen minnow spe- not within, individuals and was either orange cies were unsuitable hosts. Nine other fish spe- or white. In the field, we observed gravid female cies, representing the families Centrarchidae, Ic- P decisum releasing conglutinates in a manner taluridae, and Percidae, were unsuitable hosts similar to E cerina and commonly observed for P decisum (Table 6). drifting conglutinates in the water column. In the field, we observed schools of blacktail shin- Quadrula asperata ers, Cyprinella venusta, interacting with conglu- tinates as described for E cerina. In the labora- Quadrula asperata is a short-term brooder and tory, we presented conglutinates to minnows was gravid from spring to early summer. We 86 W. R. HAAG AND 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 glochidia from 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 before completion of the trial. - = the fish species was not used in the trial. na = not applicable.

Mean no. juveniles/fish (n)

Days to transformation Days to rejection (M)

Fishes’ A R C D A B C D Hosts ClJprimG7 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 hosts Lfuilzrs chrysocrphnlus 0 (3) 0 (0) 2 (5) 1 (1) na (0) 2-13 (4) na (0) 10 (2) 23” na 17-21 17

I Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not produce juvenile 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), Lrpomis c~yne~hs (1, 3, 6), I.. rrfacrochirus (1, 2,2), I.. mega:nlotis (2, 1.5,2), Micropterus sn2nzoides (2, 3.5,2-15), Ethmstonzn avksiar (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 bound and found mature glochidia from 17 June to 28 in this mucus. In dissected individuals, mucus July. In the laboratory, mature glochidia were re- was also associated with glochidia inside the leased freely and were not contained in conglu- gills. Long strands of mucus often issued from tinates. 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 glochidia from 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 before completion of the trial. - = the fish species was not used in the trial. na = not applicable.

Mean no. juveniles/fish (M)

Days to transformation Days to rejection (~7)

Fishes’ A B C A B C Hosts lctnlflrlrs pllilctntlrs 4 (6) o* (3) 2 (5) na (0) na (0) na (0) 25-27 22* 17-34 Marginal hosts Noturus kptacnntlm 0 (0) 0 (0) 1 (1) 3 (2) 2 (2) 26 (1) na nn 31

’ Fish species (number of trials, mean number of fish per trial, range of days to rejection) that did not produce juvenile 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), Annmmypto mrridima (1, 2, 4), Etlmslom rqmtrr~ (2, 3.5, 2-6), Pmim nigrOJmintn (2, 2.5, 3-4), )? scim (1, 2, 3-6) 20031 M USSEL HOSTS AND INFECTION Sl’RA1‘EC1ES 87 lar to Elliptio I~I’CII. Immature glochidia and eggs this trait is highly conserved at lower taxonomic were released in irregular clusters, as described levels and may be highly predictable among for E. nrca. closely related mussel species. Glochidia of Q. aspmta transformed consis- Apparent departures from patterns of host tently on channel catfish, lcfolurcrs punctafus (Ic- use among ostensibly closely related mussel taluridae) (Table 7). One additional catfish spe- species may reflect incomplete understanding of cies, Notlrrus kptacanthrs, was a marginal host. phylogenetic relationships within these groups. One catfish species, Anwiz~rus Iiatnlis, was an un- Host use of Qundrda cy/iJdricn and Q. ir?l?rrrJnlin suitable host. Twenty-seven other fish species, is restricted to 3 minnow genera (Yeager and representing the families Catostomidae, Cypri- Neves 1986, Yeager and Saylor 1995, respective- nidae, Centrarchidae, Fundulidae, and Percidae, ly), departing widely from host-use patterns of were unsuitable hosts for Q. asprmta (Table 7). other species of Quadrlrh. However, recent work showed that these 2 species are members of a monophyletic &de distinct from other mem- Discussion bers of the genus (Serb et al. 2003). Similarly, host use of ~~rsco~raia ~br1117 (restricted to skipjack herring, Ahtl chrysoclhris, Cokcr et al. 1921) All 7 mussel species in our study were host differs from other species of FJnscorJaitl but, as specialists, with host use restricted to a single currently recognized, this genus is polyphyletic family or genus of fishes. Host use for most spe- and E r+rrzn is not closely related to other mem- cies was concordant with host information ob- bers of the genus (Lydeard et al. 2000). Elliptic> tained by laboratory infection trials for closely is a large genus with most species occurring in related species. For example, primary host use coastal streams on the Atlantic slope or eastern of Ellipfio dilatata is limited to darters and scul- Gulf of Mexico (Davis et al. 1981); species from pins (Luo 1993), similar to E. nrcn, which uses these drainages use sunfishes (Centrarchidae) only darters; sculpins do not occur in the Sipsey or yellow perch (Pica ~7clirsc~1s) as hosts (E. and Buttahatchee rivers (Boschung 1989). Hosts comp/aru?fa, Matteson 1948; E. buckkyi and E. ic- for Fusconaia COY and F C~AMPO~~S include a wide krina, Keller and Rues&r 1997), in contrast to variety of minnows (Neves 1991, Bruendcrman E. NT~I and E. dilntafa from interior streams in and Neves 1993, respectively), and are similar the Mobile and Mississippi basins, respectively. to F: ccrina. Host use of MPdimidm cmrndicus, M. Differences in host use between these species pmicillatus, and a small-stream population of M. groups provide evidence for divergent phylo- acutissinnrs is restricted to darters (Zale and Ne- genetic lines within Elliptic. ves 1982, O’Brien and Williams 2002, and Haag Other apparent departures from well-estab- and Warren 1997, respectively) and is similar to lished phylogenetic patterns of host use are like- large-stream populations of M. acufissirmrs. Host ly a result of differences in host-identification use of hmpsi/is or&n is restricted to Micropferlrs methods among studies. Many host relation- spp., similar to a large number of other species ships reported in the early literature were based of Lampsilis (reviewed in Haag et al. 1999). Host on observations of natural infestations only and use of P/cmhwrn decision is similar to 7 other were not confirmed by laboratory transforma- species of IJk’1~rohCJJJ17 (I? ch7, I? COCCiJlCUJJ1, I? col- tion experiments. Most glochidia attach readily /Iran, I? cordatnm, f?flfilrzflrrJl, I! OIJ@‘JJ~C~, and I! p/r- to nonhost-fish species but are later rejected, so iformc), for which host use is restricted mostly such observations potentially result in erroneous to minnows (C)‘Dee and Watters 2000, Hove et host relationships. Furthermore, in some casts, al. 1997, Hove and Neves 1994, Yokcly 1972, these relationships are based on probable mis- Haag and Warren 1997, Weaver et al. ‘1991, identifications of encysted glochidia (see ac- O’Brien and Williams 2002, respectively). Host count for E!/ipfio crassidcrJs in Brim Box and Wil- information based on laboratory trials for close liams 2000). Host information based on a wide relatives of Qzradrh nsywnfn is available only for variety of methods has been summarized in Q. ~robilis and Q. pfrshrkxa, for which host use is several reviews (Fuller 1974, Hoggarth 1992, similar (catfishes: Howclls 1997, Coker et al. Watters 1994). Despite cautionary statements by 1921, respectively). The similarity of host LISA these authors, circumstantial or potentially er- among congeneric mussel species indicates that roneous host relationships reported in these re- 88 W. R. HAAG AND M. L. WARREN [Volume 22 views have been widely and uncritically cited 1994, Haag and Warren 1997). It is hypothesized (e.g., Parmalee and Bogan 1998). We stress the that this strategy facilitates host infection need to critically examine original sources of through the ingestion of conglutinates by small host information and methods of study before fishes, but observations of conglutinate release making and reporting conclusions about mussel and interactions with fishes in the wild are rare host use. (but see Jones et al. 1986). In the laboratory, we observed a large number of fish species, includ- ing Host-attraction strategies many unsuitable hosts, feeding on or oth- erwise interacting with conglutinates in ways The mussel species in this study used a di- that could result in glochidial transmission. In verse array of strategies for infecting host fishes contrast, in the field, we observed interactions with glochidia. Two previously described host of conglutinates of both mussel species only strategies, lure-displaying host-specialists and with the blacktail shiner, Cyprinella venusta, a conglutinate-producing host-specialists (Haag primary host for both species. Cyprinella zwusta and Warren 1998), are represented in this group occurs most commonly in the mid-water col- of species but, for 3 species, the method of host umn in moderate to swift riffles (Baker and infection was unclear. Ross 1981), and most food items are taken from Lure-displaying host-specialists were repre- the drift (Ross 2001). Based on the prevalence of sented by Medionidus acutissimus and Larnpsilis infestations of wild fishes, Bruenderman and ornata. In this strategy, gravid females display Neves (1993) hypothesized that drift-feeding lures that elicit attacks from host fishes, result- minnows were the primary hosts of E cunenlus ing in host infection (Haag and Warren 1999). and I! ouifornw in Virginia. The conglutinate-re- Lures of this type have been described for sev- lease behavior we observed for E cerina and I! eral other species of Lampsilis (Kraemer 1970, deciswn resulted in conglutinates being sus- Barnhart and Roberts 1997, Haag et al. 1999). pended in the mid-water column where they Modified mantles similar to those described were vulnerable to C. venusta and other drift- here for M. acutissiml*s have been reported for feeding minnows, but less vulnerable to unsuit- M. pmicillatus (Brim Box and Williams 2000), able hosts such as darters and other benthic- and similar displays in the wild have been ob- feeding fishes. served for M. conradius (S. Ahlstedt, US Geo- Elliptio arca and Quadrula asperata displayed logical Survey, Knoxville, Tennessee, personal no modified mantle lures and did not release communication). In Lafnpsilis, large mantle lures mature glochidia in conglutinates. During han- selectively target suitable host fishes by mimick- dling, both species, as well as other short-term ing prey items of these fishes, reducing the brooders (Yeager and Neves 1986), often abort probability of infection of unsuitable fish species immature glochidia or eggs in structures resem- (Haag and Warren 2000). The modified mantle bling conglutinates, but this behavior does not of Medionidus likely has a similar function, al- represent a strategy for host attraction. Rather, though interactions with fishes have not been transmission of glochidia to hosts may be facil- observed. Because of the small size of the lure itated by entanglement of fishes in mucous and the location of displaying females within threads, which are released in association with the interstices of coarse substrates, the lure may and contain mature glochidia. Release of mucus be inconspicuous to most fishes except darters or other web-like structures in association with (the sole host for Mediorlidus), many species of glochidia has been observed in host-specialists which typically feed among gravel and cobble (Matteson 1948, Yokely 1972, Woody and Hol- substrates (Page 1983). land-Bartels 1993) and host-generalists (Lefevre Conglutinate-producing host-specialists were and Curtis 1910, Wood 1974, Haag and Warren represented by Fuscormia cerina and Pleurobel~ln 1997). Such a strategy would be effective for &C~SUI?I. In this strategy, females release glochid- generalists because a wide variety of fishes like- ia in small packets, which resemble food items ly would be infected indiscriminately. For host- of small, predaceous fishes such as darters and specialists, such a strategy seems maladaptive minnows. This strategy is known for several because the likelihood of infection of nonhost other species of F~sconnin and PI~urobcnzn fishes and subsequent loss of these offspring (Bruenderman and Neves 1993, Hove and Neves would be high. Our observations of glochidial 20031 MUSSEL HOSTS AND INFECTION STRATEGIES 89 release by E. arca and Q. asyernta were made species use common, widespread fishes as only in the laboratory and may not be represen- hosts. Pleurobema decisurn, a federally endan- tative of release behaviors in the wild. Field ob- gered species, consistently used only one fish servations are needed to fully elucidate host-at- species, Cyprinella venusta, as host. Although in traction strategies for these species. some cases, use of only one fish species may be We made no observations of Obovaria unicolor considered a conservation liability, C. venusta is in the field or laboratory that suggested poten- one of the most widespread and abundant fish- tial host-attraction strategies for this species. es in the western Mobile Basin (Boschung 1989, Animals did not display mantle lures, did not Ross 2001). Furthermore, C. venusta is tolerant produce conglutinates, and did not release mu- of highly degraded habitats including impound- cus in association with glochidia. Glochidia ed and channelized streams (Mettee et al. 1996, were brooded only in the posterior portion of Ross 2001). Medionidus acutissimus, a federally the outer gills and were not associated with mu- threatened species, uses many darter species as cus or any conglutinate structure. These brood- hosts, including abundant and widespread spe- ing traits are shared with the genera Epioblasma, cies such as Percina nigrofasciata. Obovaria unicolor Medionidus, Lampsilk, Ligumia, Toxolama, and has experienced a dramatic recent decline in the Villosa, all of which display lures. It is therefore Buttahatchee River (Hartfield and Jones 1990, possible that 0. unicolor possesses a lure that we Jones 1991). We have no data on current popu- did not observe. However, in lure-displaying lation levels of sand darters and Etheostoma ar- species, modified mantle margins that compose tesiae (hosts for 0. unicolor) in the Buttahatchee the lures are visible even when the lure is not River, but these fishes are currently widespread displayed (Haag et al. 1999); such a structure and common in other tributaries of the Tombig- was not evident in 0. unicolor. Obovaria unicolor bee River in Alabama and Mississippi (Mettee was found in close association with its primary et al. 1996, Ross 2001, MLW and WRH, unpub- fish host; both 0. unicolor and sand darters (Am- lished data). Clearly, factors other than loss of mocrypta spp.) occur most frequently in clean or fish hosts (e.g., altered flows, habitat loss, water- silty sand in low-flow areas (Ross 2001, WRH quality degradation) are responsible for declines and MLW, unpublished data). Sand darters feed of these and other freshwater mussels in the mostly on midge larvae (Diptera), but also in- Mobile Basin. gest other small prey, including larval Asian clams (Covbicula,f7uminea) (Ross 2001). Glochidia Acknowledgements broadcast in this habitat may have a high like- lihood of being encountered and ingested by We thank J. G. McWhirter, A. Greer, J. L. Sta- foraging sand darters. However, no North ton, T. Fletcher, T. Slack, T. Mann, I? Hartfield, American mussel species are currently known A. Sheldon, J. Layzer, C. Lydeard, D. Carlson, to broadcast glochidia and rely on passive in- C. Jenkins, and E McEwen for their various con- fection of host fishes; rather, all well-studied tributions to this study. This study was sup- species exhibit some type of strategy to facilitate ported by the Mississippi Wildlife Heritage host infection. Further field and laboratory ob- Fund and the Southern Research Station, US De- servations are needed to determine the host-in- partment of Agriculture, Forest Service. fection mode for this species. Literature Cited ltq~lications for conservatio~7 CAKIER, J. A., ANI) S. T. Ross. 1981. Spatial and tem- Mussel populations in the Mobile Basin, as in poral resource utilization by southeastern cypri- most of North America, have declined over the nids. Copeia 1981:178-189. M. C., AND A. 1997. Reproduc- last 30 y (Neves et al. 1997). In some rivers, de- BARNHART, ROIXI?TS. tion and fish hosts of unionids from the Ozark clines in mussel populations are attributed to uplifts. Pages 15-20 irl K. S. Cummings, A. C. disappearance or declines of host fishes, result- Buchanan, C. A. Mayer, and T. Naimo (editors). ing in reduced mussel reproductive success Conservation and management of freshwater (Smith 1985, Khym and Layzer 2000). This mussels II: Initiatives for the future. Upper Mis- mechanism is insufficient to explain declines of sissippi River Conservation Committee, Rock Is- the 7 mussel species in this study because all land, Illinois. 90 W. R. HAAG AND M. L. WARREN [Volume 22

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