Songbird Dispersal of American ginseng (Panax quinquefolius)

Songbird Dispersal of American ginseng (Panax quinquefolius) Author(s): Amy M. Hruska, Sara Souther, James B. Mcgraw Source: Ecoscience, 21(1):46-55. Published By: Centre d'études nordiques, Université Laval DOI: http://dx.doi.org/10.2980/21-1-3679 URL: http://www.bioone.org/doi/full/10.2980/21-1-3679

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James B. MCGRAW,'HSDUWPHQWRI%LRORJ\:HVW9LUJLQLD8QLYHUVLW\ 0RUJDQWRZQ:HVW9LUJLQLD86$ Abstract: American ginseng (Panax quinquefolius  LV DQ XQFRPPRQ SHUHQQLDO XQGHUVWRU\ KHUE IRXQG LQ HDVWHUQ GHFLGXRXV forest. The species is harvested for the international medicinal plant trade. While previous research has inferred that seed GLVSHUVDO LV OLPLWHG WKH SURGXFWLRQ RI EULJKW UHG IOHVK\ EHUULHV VXJJHVWV ORQJGLVWDQFH GLVSHUVDO PD\ EH IDFLOLWDWHG E\ VRQJELUGV7KHREMHFWLYHRIWKLVVWXG\ZDVWRGHWHUPLQHKRZVRQJELUGVLQWHUDFWHGZLWKJLQVHQJDQGZKHWKHUWKH\GLVSHUVHG or predated ginseng seeds. We used infrared, motion-activated cameras to observe animal–ginseng interactions in the field. To determine the disperser potential of songbirds observed visiting ginseng in the field, we conducted a captive feeding VWXG\ DW WKH 7HQQHVVHH$TXDULXP 7KUXVKHV UHPRYHG EHUULHV IURP JLQVHQJ LQIUXFWHVFHQFHV PRUH IUHTXHQWO\ FRPSDUHG WR RWKHUSRWHQWLDOGLVSHUVHUVDQGUHJXUJLWDWHGYLDEOHVHHGV±PLQXWHVDIWHULQJHVWLRQLQIHHGLQJWULDOV%\GLVSHUVLQJJLQVHQJ VHHGVWKUXVKHVSURYLGHDPHFKDQLVPIRUJLQVHQJWRLPSURYHLWVSUREDELOLW\RISHUVLVWHQFHLQWKHIDFHRISULPDU\WKUHDWVWR populations: deer browse, harvest, and climate change. Keywords: American ginseng, songbird dispersal, wood thrush. Résumé/HJLQVHQJjIROLROHVPanax quinquefolius) est une herbe vivace peu commune que l'on trouve dans le sous-étage des forêts feuillues de l'Est. L'espèce est récoltée pour le commerce international des plantes médicinales. De précédentes recherches ont suggéré que la dispersion des graines de cette plante est limitée. Cependant, la production de baies charnues rouge vif laisse croire que la dispersion des graines sur de longues distances pourrait être facilitée par les oiseaux chanteurs. L'objectif de cette étude était d'examiner la nature des interactions entre les oiseaux chanteurs et le ginseng et de déterminer si les oiseaux représentent des agents de dispersion ou des prédateurs pour les graines du ginseng. Nous avons utilisé des caméras infrarouges activées par le mouvement pour observer les interactions oiseau-ginseng sur le terrain. Afin de connaître le potentiel des oiseaux chanteurs comme agent de dispersion du ginseng, nous avons réalisé des essais d'alimentation avec des oiseaux en captivité à l'aquarium du Tennessee. Ce sont les grives qui récoltaient le plus souvent les baies d'infructescences du ginseng, comparées à d'autres agents potentiels de dispersion, et elles régurgitaient des graines viables GHjPLQXWHVDSUqVO LQJHVWLRQGDQVOHVHVVDLVG DOLPHQWDWLRQ(QGLVSHUVDQWOHVJUDLQHVGXJLQVHQJOHVJULYHVIRXUQLVVHQW XQ PpFDQLVPH SHUPHWWDQW j FHWWH SODQWH G DPpOLRUHU VD SUREDELOLWp GH SHUVLVWDQFH IDFH j  PHQDFHV SULQFLSDOHV SRXU VHV populations : le broutement par le cerf, la récolte et les changements climatiques. Mots-clésGLVSHUVLRQSDUGHVRLVHDX[FKDQWHXUVJLQVHQJjIROLROHVJULYHGHVERLV Nomenclature.DUWH]:LOVRQ 5HHGHU$PHULFDQ2UQLWKRORJLVWV¶8QLRQ

Introduction American ginseng (Panax quinquefolius) is a forest herb found throughout much of eastern North America’s deciduous forests. The species is well known for its mediFLQDO SURSHUWLHV -RKDQQVHQ  $QQXDOO\ KXQGUHGV of thousands of wild ginseng roots are harvested and sold into the international medicinal plant trade (Division of 0DQDJHPHQW$XWKRULW\   JHQHUDWLQJ PLOOLRQV RI GROODUVLQVXSSOHPHQWDOLQFRPHIRUKDUYHVWHUV5REELQV  Concerns about overharvest of ginseng led to its listing on Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES)

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5HFDFF Associate Editor: Daniel Gagnon. 2 Author for correspondence. '2,

in  DQG UHVXOWHG LQ PRQLWRULQJ RI WKH LQWHUQDWLRQDO H[SRUWRI$PHULFDQJLQVHQJURRWV5REELQV  In addition, American ginseng is a long-lived, perennial herb found in thousands of small populations throughout $SSDODFKLDQ IRUHVWV WKDW DUH FKDUDFWHUL]HG E\ D FOXVWHUHG spatial distribution of individuals within populations 0F*UDZ 6DQGHUV  9DQ GHU 9RRUW  &UXVH6DQGHUV +DPULFND 'XHWRLWVHFRQRPLFLPSRUWDQFHDOLIH F\FOH VLPLODU WR PDQ\ RWKHU XQGHUVWRU\ KHUEV DQG LWV ZLGH spatial distribution comprised of thousands small populations, American ginseng has become a model species for investigating a plethora of demographic and conservationbased questions. Extensive research has been conducted LQYHVWLJDWLQJ WKH GHPRJUDSK\ RI$PHULFDQ JLQVHQJ DQG how various environmental factors influence individual plant performance (reviewed in McGraw et al.   These research studies have found that in addition to the

ÉCOSCIENCE, VOL. 21 (1), 2014

QHJDWLYH LPSDFWV RI JLQVHQJ KDUYHVW GHHU KHUELYRU\ DQG FOLPDWHFKDQJHDUHHQYLURQPHQWDOIDFWRUVDOVRQHJDWLYHO\ impacting the population growth of ginseng (reviewed in McGraw et al. +RZHYHUDFULWLFDODVSHFWRIJLQVHQJ GHPRJUDSK\WKDWUHPDLQVSRRUO\XQGHUVWRRGLVLWVGLVSHUVDO &UXVH6DQGHUV +DPULFNDE0F*UDZ et al.  Dispersal influences the spatial distribution, gene flow, and evolution of a species. Seed dispersal increases the GLVWDQFH EHWZHHQ SDUHQW DQG RIIVSULQJ WKHUHE\ UHGXFLQJ competition and disease transmission between the parent and offspring, and among siblings, as well as decreasing other intraspecific interactions between individuals ZLWKLQ D SRSXODWLRQ $XJVSXUJHU   'LVSHUVDO UHGXFHV inbreeding with relatives, but in species such as ginseng WKDW GLVSOD\$OOHH HIIHFWV +DFNQH\  0F*UDZ   LW PD\LVRODWHLQGLYLGXDOVIURPSRWHQWLDOPDWHVLQFUHDVLQJWKH degree of selfing. Seed dispersal also facilitates the expansion of a population as well as the establishment of new SRSXODWLRQV +RZH  6PDOOZRRG  &ODUN  &ODUN &ODUN et al. 5HFHQWFRQFHUQVRYHUWKHSRWHQWLDO for populations and species to shift distribution in response to changing climate have highlighted the need for a comprehensive investigation of plant dispersal mechanisms (e.g., 3HDUVRQ  'DZVRQ  7KXLOOHU et al.  (QJOHU  *XLVDQ  $PHULFDQ JLQVHQJ LV D VSHFLHV DGDSWHG WR local temperature conditions, and determining its dispersal mechanisms is important for understanding both the current and future distributions of populations (Souther & McGraw,  'LVSHUVDODZD\IURPGHHUWUDLOVRUWRQHZVLWHVDZD\ IURPSRSXODWLRQVNQRZQE\KXPDQKDUYHVWHUVFRXOGDOVREH important to persistence of ginseng. To date, American ginseng seeds have been conVLGHUHG WR EH JUDYLW\ GLVSHUVHG /HZLV  =HQJHU  9DQ GHU 9RRUW   *UDYLW\ GLVSHUVDO UHVXOWV LQ VKRUW distance dispersal events for plant species and is often combined with one or more other dispersal mechanisms 9LWWR] (QJOHU $PHULFDQJLQVHQJSURGXFHVIOHVK\ red berries, suggesting animal-facilitated seed dispersal +RZH  6PDOOZRRG  0F*UDZ et al.   7KH EHVWGRFXPHQWHG JLQVHQJ±DQLPDO LQWHUDFWLRQ LV E\ ZKLWH tailed deer (Odocoileus virginianus). However, feeding trials showed that seeds were rendered inviable when berULHVZHUHLQJHVWHG)XUHGL 0F*UDZ 2WKHUJLQVHQJ VHHG±DQLPDO LQWHUDFWLRQV KDYH RQO\ EHHQ WKH VXEMHFW RI DQHFGRWHV WKRXJK SKHQRORJ\ DQG PRUSKRORJLFDO FKDUDFWHULVWLFVRIJLQVHQJEHUULHVVXJJHVWVRQJELUGVPD\IDFLOLWDWH JLQVHQJGLVSHUVDO3ULWWV  *UHHQ JLQVHQJ EHUULHV EHJLQ WR IRUP LQ PLG-XO\ and ripen to red throughout August and September (McGraw et al.   :KLOH VRPH VRQJELUGV DUH IUXJLYRURXV \HDUURXQG PDQ\ PLJUDWRU\ VRQJELUGV VZLWFK IURP an insectivorous diet to a frugivorous diet during the fall prior to migration, resulting in an increased demand for IUXLWV 6WLOHV  ,]KDNL  6DIULHO  $GGLWLRQDOO\ VRQJELUGV DUH SDUWLFXODUO\ DWWUDFWHG WR IUXLWV WKDW KDYH D strong contrast against foliage, resulting in a diet of fruits WKDW DUH SULPDULO\ SXUSOH UHG RU EODFN LQ FRORXU 6FKPLGW  6FKDHIHU  ,OX]   *LQVHQJ EHUULHV FRQWDLQ ± VHHGV DQG ZKHQ ULSH FDQ UDQJH IURP  WR  PP LQ VL]H ZLWK VHHGV WKDW DUH OHVV WKDQ  PP 7KH DELOLW\ RI

frugivorous bird species to ingest fruit has been shown to EH OLPLWHG E\ WKH ZLGWK RI WKH JDSH SDUWLFXODUO\ IRU VSHcies that gulp, or ingest, the whole fruit (Wheelwright,  3LSHU  -RUGDQR  /HYH\  /DPEHUW   7KH VPDOO VL]H RI$PHULFDQ JLQVHQJ VHHGV ZRXOG WKHRUHWLFDOO\ DOORZ WKHP WR EH LQJHVWHG E\ D PDMRULW\ RI VRQJELUGVSHFLHVZLWKLQLWVUDQJH0H\HU :LWPHU  Furthermore, ginseng seeds have a hard exterior coat that PD\SUHYHQWGDPDJHWRWKHHPEU\RDIWHULQJHVWLRQDQGSRVVLEO\ HQDEOH LW WR SDVV WKURXJK D ELUG¶V JL]]DUG &RXVHQV '\WKDP /DZ  7KH RYHUDOO REMHFWLYH RI WKLV VWXG\ ZDV WR LQYHVWLJDWH songbirds as potential seed dispersers of American ginseng. 6SHFLILFDOO\ZHDVNHG :KDWLVWKHIUHTXHQF\DQG³LQWLPDF\´ RI DQLPDO±JLQVHQJ LQWHUDFWLRQV SDUWLFXODUO\ VRQJELUG interactions? 2) What proportion of berries is removed as WKHUHVXOWRIJLQVHQJ±DQLPDOLQWHUDFWLRQV" ,VWKHUHDGLIIHUHQFH LQ WKH IUHTXHQF\ DQG ³LQWLPDF\´ RI DYLDQ±JLQVHQJ interactions compared to mammalian–ginseng interactions? 4) Of the avian interactions, what songbird species most freTXHQWO\LQWHUDFWZLWKJLQVHQJ" 'RVRQJELUGVWKDWLQWHUDFW with ginseng defecate or regurgitate viable seeds? 6) How ORQJ GR JLQVHQJ VHHGV VWD\ ZLWKLQ D VRQJELUG¶V GLJHVWLYH V\VWHP" 7KH DQVZHUV WR WKHVH TXHVWLRQV SURYLGH FULWLFDO information regarding how ginseng is dispersed across the ODQGVFDSHDQGXOWLPDWHO\FDQEHXVHGWRFUHDWHPRUHDFFXUate demographic models of ginseng.

Methods FIELD INVESTIGATION OF SONGBIRD–GINSENG INTERACTIONS To determine whether songbirds interact with American ginseng and how close their interactions are, 0RXOWULH ' %LUPLQJKDP$/ 86$  LQIUDUHG PRWLRQ activated wildlife cameras were placed within 6 wild ginseng populations near Morgantown, West Virginia from  WR  WRWDO SRSXODWLRQV\HDU        2QH WR  FDPHUDV ZHUH set up per site in mid-August, once berries began to ripen from green to red. Most often, cameras were removed once berries were absent from the infructescence or the plant had VHQHVFHG :LOGOLIH FDPHUDV ZHUH SRVLWLRQHG RQ P WDOO  î FP FDPRXIODJHSDLQWHG ZRRGHQ VWDNHV DW D GLVtance of 1–2 m from a focal reproductive plant or cluster of reproductive plants within a population. Cameras could be WULJJHUHG DQG UHFRUG LPDJHV DW DQ\ WLPH GD\ RU QLJKW )RU HDFK LQVWDQFH WKDW D FDPHUD ZDV WULJJHUHG E\ DQ LQIUDUHG PRYHPHQWWKHZLOGOLIHFDPHUDVZHUHVHWWRWDNHLPDJHV 7KHVH  LPDJHV ZHUH XVHG WR GHILQH D VLQJOH SRWHQWLDO GLVpersal event. The cameras were also programmed to have a PLQGHOD\EHWZHHQHDFKRIWKHVHHYHQWV Potential dispersers were identified within each event, and a value was assigned to the event that corresponded to the level of interaction a potential disperser had with the focal ginseng plant(s). Events were categorized based on D ± VFDOH ZKHUH  UHSUHVHQWHG WKH ORZHVW OHYHO RI LQWHUaction, no apparent potential disperser within the image EXWVRPHWKLQJWULJJHUHGWKHFDPHUD DQGUHSUHVHQWHGWKH KLJKHVW OHYHO ZLWK EHUULHV FOHDUO\ UHPRYHG E\ WKH SRWHQtial disperser from the ginseng infructescence (Table I). 47

HRUSKA, SOUTHER & MCGRAW: SONGBIRD DISPERSAL OF AMERICAN GINSENG

TABLE,(DFKLQWHUDFWLRQHYHQWPDGHXSRIDVHULHVRILPDJHVSHULQIUDUHGPRWLRQDFWLYDWHGRFFXUUHQFHZDVDVVLJQHGDTXDQWLWDWLYHYDOXH to represent the level of interaction a potential disperser (PD) had with American ginseng berries. Level of interaction

Value

Description

1RQH



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/RZ  

  

7KH3'LVLQSKRWRJUDSKDQGQRWXQGHUWKHFDQRS\a of the ginseng plant for 2 or more images. 7KH3'LVXQGHUWKHFDQRS\aRIWKHJLQVHQJSODQWIRUHLWKHURULPDJHVEXWLWLVQRWIRUDJLQJb. 7KH3'LVXQGHUWKHFDQRS\RIWKHSODQWLQTXHVWLRQIRUHLWKHURULPDJHVDQGLVIRUDJLQJb.

High   

4   

The PD has touched the infructescence. $EHUU\JRHVPLVVLQJEHWZHHQHYHQWVZLWKDWOHDVWRIWKHHYHQWVKDYLQJDQLGHQWL¿DEOH3' 7KHUHLVDEHUU\LQWKH3'¶VSRVVHVVLRQ :LWKLQWKHWKUHHLPDJHVHTXHQFHRIDQHYHQWDEHUU\KDVEHHQUHPRYHGIURPWKHLQIUXFWHVFHQFH

a b

8QGHUFDQRS\WKHSRWHQWLDOGLVSHUVHUDSSHDUVEHORZWKHOHDYHVRIWKHIRFDOJLQVHQJSODQW Foraging: the potential disperser has its nose or beak to the ground below the leaves of the focal ginseng plant.

2QO\ LPDJHV ZKHUH D SRUWLRQ RI RU DOO EHUULHV KDG ULSHQHG ZHUH XVHG IRU FDOFXODWLRQV DQG DQDO\VHV 6XPPDU\ VWDWLVWLFV LQFOXGHG   PHDQ QXPEHU RI HYHQWV SHU FDPHUDGD\  IUHTXHQF\RISRWHQWLDOGLVSHUVHUVZLWKLQDJLYHQOHYHORI LQWHUDFWLRQ SURSRUWLRQRIHYHQWVZLWKQRYLVLEOHSRWHQWLDO disperser, 4) proportion of berries missing per plant after a OHYHO  RU  LQWHUDFWLRQ ZLWK D SRWHQWLDO GLVSHUVHU   WRWDO proportion of overall potential dispersers that were avian or mammalian, and 6) proportion of potential dispersers that were avian and mammalian per level of interaction. For those events containing a potential disperser, a log-likeliKRRG DQDO\VLV ZDV SHUIRUPHG XVLQJ 6$6 -03 6WDWLVWLFDO 6RIWZDUHY6$6,QVWLWXWH&DU\1RUWK&DUROLQD86$  to determine whether avian potential dispersers more freTXHQWO\ KDG KLJKOHYHO LQWHUDFWLRQV ZLWK JLQVHQJ FRPSDUHG WR PDPPDOLDQ SRWHQWLDO GLVSHUVHUV $GGLWLRQDOO\ JLYHQ WKH W\SHV RI DYLDQ SRWHQWLDO GLVSHUVHUV REVHUYHG ZLWKLQ WKH LPDJHV D VHFRQG ORJOLNHOLKRRG DQDO\VLV FRPSDUHG WKH OHYHO RI LQWHUDFWLRQ WKDW WKUXVK VSHFLHV IDPLO\ 7XUGLGDH  and non-thrush avian potential dispersers had with ginseng. Thrush species that could have been observed in the field included American robin (Turdus migratorius  JUD\FKHHN thrush (Catharus minimus), hermit thrush (Catharus guttatus), Swainson’s thrush (Catharus ustulatus), wood thrush (Hylocichla mustelina DQGYHHU\Catharus fuscescens). INVESTIGATION OF THRUSHES AS POTENTIAL DISPERSERS Based on the field observation of thrushes as one of the most frequent potential avian dispersers, feeding trials were conducted with 4 captive thrushes at the Tennessee $TXDULXP IURP 6HSWHPEHU  WR   2YHU WKH FRXUVH RI  G JLQVHQJ EHUULHV ZHUH IHG ad libitum to a hermit WKUXVK D 6ZDLQVRQ¶V WKUXVK D YHHU\ DQG D ZRRG WKUXVK Due to renovations to their normal exhibit, the hermit WKUXVK 6ZDLQVRQ¶V WKUXVK DQG YHHU\ ZHUH PDLQWDLQHG LQ D FDJHHQYLURQPHQWîîFP DQGKDGEHHQOLYing there for 4 weeks. While the hermit thrush was placed LQ D FDJH E\ LWVHOI WKH 6ZDLQVRQ¶V WKUXVK DQG YHHU\ ZHUH FDJHGWRJHWKHUGXHWRVSDFHOLPLWDWLRQV$GGLWLRQDOO\GXHWR space limitations, the wood thrush could not also be caged, and feeding trials for this species were conducted within WKH³'HOWD&RXQWU\([KLELW´ca P2), which included vegetation as well as other bird species. 

%HUU\ SURGXFWLRQ LV ORZ LQ QDWXUDO SRSXODWLRQV VR ginseng berries for feeding trials were obtained from a JLQVHQJ FXOWLYDWRU XVLQJ ³ZRRGV JURZQ´ JURZWK PHWKRGV XQGHUQDWXUDOWUHHFDQRS\ %HUULHVZHUHFROOHFWHGGLUHFWO\ from plants 2 d prior to the feeding trials and were stored at 4 °C. Ginseng berries were offered detached from infructesFHQFHVZLWKLQIHHGLQJWUD\VGXULQJWKHQRUPDOIHHGLQJWLPH  WR   'XULQJ WKH ILUVW GD\ DQG IRU WKH PRUQLQJ RIWKHVHFRQGGD\EHUULHVZHUHRIIHUHGVLPXOWDQHRXVO\ZLWK normal food items (mealworms, sunflower seeds, etc.) in RUGHU WR PLQLPL]H VWUHVV WR WKH ELUGV LQ FDVH WKH\ UHMHFWHG the fruit. Berries were offered as the sole food item for the UHPDLQLQJWULDOVGXULQJWKHDIWHUQRRQRIWKHVHFRQGGD\DQG WKHPRUQLQJRIWKHWKLUGGD\DIWHUELUGVKDGEHHQREVHUYHG ingesting the berries. Within the exhibit that held the wood thrush, at least 2 observers were present to record wood thrush feeding behaviour, given that the bird still had free movement ZLWKLQ WKH H[KLELW DQG RWKHU VSHFLHV WKDW FRXOG SRWHQWLDOO\ eat the berries were present. Video cameras were used to UHFRUG WKH EHKDYLRXU RI WKH FDJHG ELUGV 3ULPDU\ REVHUvations were made regarding the digestive behaviours (whether seeds were defecated or regurgitated) of the thrushes and the amount of time between ingestion and an exhibited digestive behaviour. Additional observations were made regarding the total number of berries that were eaten E\HDFKELUGWKHSURSRUWLRQRIRQHVHHGHGDQGWZRVHHGHG berries eaten, and, in the wood thrush exhibit, the number RI RWKHU DYLDQ VSHFLHV WKDW LQWHUDFWHG ZLWK DQG WKH W\SH RI LQWHUDFWLRQV WKH\ KDG ZLWK WKH JLQVHQJ EHUULHV 5HFRYHUHG VHHGVWKDWKDGEHHQLQJHVWHGZHUHWHVWHGIRUHPEU\RYLDELOLW\ XVLQJ D  WHWUD]ROLXP FKORULGH VROXWLRQ %DVNLQ  %DVNLQ 

Results FIELD INVESTIGATION OF SONGBIRD–GINSENG INTERACTIONS ,Q WRWDO  ZLOGOLIH FDPHUDV ZHUH XVHG IURP  WR UHVXOWLQJLQFDPHUDGD\VDQGDWRWDORIFDPHUDWULJJHUHG HYHQWV  WRWDO LPDJHV  :LOGOLIH FDPHUDV ZHUHWULJJHUHG“PHDQ“6( WLPHVSHUFDPHUDGD\ ZLWK D UDQJH RI ± WULJJHUHG HYHQWV SHU FDPHUDGD\ 2I WKHRULJLQDOFDPHUDVGHSOR\HGLPDJHFROOHFWLRQIRUFDPHUDV     HQGHG SUHPDWXUHO\ GXH WR

ÉCOSCIENCE, VOL. 21 (1), 2014

EDWWHU\GUDLQRUDFDPHUDPDOIXQFWLRQDQGWKHUHIRUHLPDJHV of potential dispersers were not collected after berries had ULSHQHG$GGLWLRQDOO\ D WRWDO RI  FDPHUD WULDOV ZHUH QRW DEOHWREHLQFOXGHGLQDQDO\VHVEHFDXVHPHPRU\FDUGVZHUH VWROHQ       OLNHO\ EHFDXVH RI WKH LOOHJDO KDUYHVW RI WKH IRFDO SODQWV  2I WKH WRWDO  WULJJHUHGHYHQWVHYHQWVKDGQRSRWHQWLDOGLVSHUVHU/HYHO LQWHUDFWLRQ7DEOH, KDGPDPPDOLDQSRWHQWLDOGLVSHUVHUVDQGKDGDYLDQSRWHQWLDOGLVSHUVHUV $ PDMRULW\   RI WKH HYHQWV IRU ERWK DYLDQ DQG mammalian potential dispersers were categorized as a Level 1 interaction. Of the interaction levels that involved direct interaction with a ginseng infructescence and berULHV /HYHOV  DQG   PDPPDOV ZHUH FDWHJRUL]HG PRVW IUHTXHQWO\ DV /HYHO  LQWHUDFWLRQ ZKLOH DYLDQ GLVSHUVHUV ZHUH FDWHJRUL]HG PRVW IUHTXHQWO\ DV /HYHO  LQWHUDFWLRQV (Table II). On average, 2 berries were missing from an LQIUXFWHVFHQFH IROORZLQJ D /HYHO  RU  LQWHUDFWLRQ E\ D SRWHQWLDO GLVSHUVHU IRU HYHU\  EHUULHV DYDLODEOH “  The maximum number of berries missing from focal infructescences as the result of or following Level 4 and  DYLDQ LQWHUDFWLRQV ZDV  7DEOH ,,,  ZKHUHDV  ZDV WKH maximum number missing or removed from focal infructesFHQFHV IROORZLQJ /HYHO  DQG  PDPPDOLDQ LQWHUDFWLRQV (Table III). ,Q RUGHU WR KDYH HQRXJK UHSOLFDWLRQ WR VWDWLVWLFDOO\ compare mammalian and avian dispersers, the levels of LQWHUDFWLRQ ZHUH VLPSOLILHG /HYHOV ± ZHUH FRPELQHG LQWRDVLQJOHFDWHJRU\ZHWHUP³/RZ/HYHO´EHFDXVHWKHVH included behaviours that did not involve direct interaction with the ginseng infructescence and were therefore least OLNHO\ WR UHVXOW LQ D GLVSHUVDO HYHQW /HYHOV  DQG  ZHUH FRPELQHG LQWR D FDWHJRU\ ZH UHIHU WR DV ³+LJK /HYHO´

EHFDXVH WKH\ LQFOXGHG EHKDYLRXUV LQYROYLQJ GLUHFW LQWHUDFWLRQZLWKWKHJLQVHQJLQIUXFWHVFHQFHDQGZHUHPRVWOLNHO\ to result in a dispersal event. Mammalian and avian dispersHUV ZHUH VLJQLILFDQWO\ GLIIHUHQW LQ WKH SURSRUWLRQ RI /RZ DQG+LJK/HYHOLQWHUDFWLRQVZLWKJLQVHQJEHUULHV)LJXUH OLNHOLKRRGUDWLRȤ2 p :KLOHPDPPDOLDQ SRWHQWLDO GLVSHUVHUV PRVW IUHTXHQWO\ WULJJHUHG WKH ZLOGOLIH cameras, avian potential dispersers were captured most freTXHQWO\LQWHUDFWLQJGLUHFWO\ZLWKJLQVHQJEHUULHV)LJXUH  6TXLUUHO VSHFLHV IDPLO\ 6FLXULGDH  DFFRXQWHG IRU  RI WKH  PDPPDOLDQ SRWHQWLDO GLVSHUVDO HYHQWV Eastern chipmunks (Tamias striatus) were the most frequent potential dispersers (n    IROORZHG E\ PLFH (Peromyscus VS IDPLO\ &ULFHWLGDH  n    DQG (DVWHUQ JUD\VTXLUUHOVSciurus carolinensis) (n  2IWKHPDPPDOLDQSRWHQWLDOGLVSHUVHUVRQO\FKLSPXQNVLQWHUDFWHGZLWK ginseng berries at the High Level of interaction (Figure 2), EXWIRUDJLQJEHKDYLRXUEHORZIRFDOJLQVHQJSODQWV/HYHO interaction) was observed among chipmunks and squirrels (Table II). Of the avian potential dispersers, thrush species DFFRXQWHG IRU  RI WKH  DYLDQ HYHQWV 7KH PRVW common avian potential dispersers were wood thrushes (n    IROORZHG E\$PHULFDQ URELQV Turdus migratorius) (n = 6) and hermit thrushes (n    7DEOH ,,  8VLQJ the Low and High levels of interaction, thrush species were IRXQG WR GLIIHUHQWLDOO\ LQWHUDFW ZLWK JLQVHQJ UHODWLYH WR RWKHUDYLDQSRWHQWLDOGLVSHUVHUVOLNHOLKRRGUDWLRȤ2  p    DQG ZHUH IRXQG WR PRVW IUHTXHQWO\ LQWHUDFW ZLWKWKHLQIUXFWHVFHQFHDQGEHUULHV)LJXUH 7KHWKUXVK species that were found to interact with the infructescence and ginseng berries were wood thrushes (n = 7), hermit thrushes (n = 2), and a Swainson’s thrush (n  )LJXUH 

TABLE II. The total number of events for each mammalian and avian species per levels of interaction. Level of interaction 'LVSHUVHUW\SH 0DPPDOLDQ   



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(DVWHUQFKLSPXQN 0RXVHPXOWLSOHVS  (DVWHUQJUD\VTXLUUHO Raccoon Virginia opossum White-tailed deer )R[VTXLUUHO Fisher Weasel Cotton-tail rabbit

   21 17 6  2 2 1

(DVWHUQFKLSPXQN  (DVWHUQJUD\VTXLUUHO  0RXVHPXOWLSOHVS   Virginia opossum 1

 6     1 1 1

:RRGWKUXVK Crow    

 :RRGWKUXVK American robin 2YHQELUG +HUPLWWKUXVK 8QLGHQWL¿HGWKUXVK 7XUNH\ Eastern towhee Tufted titmouse Cardinal 

High

(DVWHUQFKLSPXQN (DVWHUQJUD\VTXLUUHO )R[VTXLUUHO





  

(DVWHUQFKLSPXQN 

  1    



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:RRGWKUXVK

   

   







  



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:RRGWKUXVK Hermit thrush 6ZDLQVRQ VWKUXVK

 2 



49

HRUSKA, SOUTHER & MCGRAW: SONGBIRD DISPERSAL OF AMERICAN GINSENG

TABLE III. The total number of berries removed per camera locaWLRQIROORZLQJD/HYHORULQWHUDFWLRQZLWKDSRWHQWLDOGLVSHUVHU DQG WKH VSHFLHV UHVSRQVLEOH IRU WKH EHUU\ UHPRYDO DW HDFK FDPera location, where n is the number of berries missing due to an animal interaction. %HUULHV removed

%HUU\ total

FCF1 73:

6 

6 

73*





   1        1$

   2        1$

Camera ID

)&) )&) $) AF1 :/ 3 73 735 73: 735& :/ 735

Interacting species Wood thrush (n = 6) :RRGWKUXVKn  Hermit thrush (n = 1) 6ZDLQVRQ¶VWKUXVKn = 1) Eastern chipmunk (n = 1) :RRGWKUXVKn = 2) +HUPLWWKUXVKn = 1) (DVWHUQFKLSPXQNn = 1) Eastern chipmunk (n = 1) (DVWHUQFKLSPXQNn = 1) 1$ 1$ 1$ 1$ 1$ 1$ 1$

HLI

1

LLI

Proportion of events

likelihood ratio: Ȥ2 = 19.88, p < 0.0001 0.8

Discussion

0.6 0.4 0.2 0

Avian 0

25

Mammalian 50

75 100 125 150 175 200 225 250 275 Number of events

FIGURE 1. Partitioning of avian and mammalian potential disperser events EDVHG RQ FDWHJRULHV WKDW ZRXOG OHDVW OLNHO\ UHVXOW LQ D GLVSHUVDO HYHQW //,/RZ/HYHORI,QWHUDFWLRQ DQGPRVWOLNHO\UHVXOWLQDGLVSHUVDOHYHQW (HLI: High Level of Interaction).

INVESTIGATION OF THRUSHES AS POTENTIAL DISPERSERS 2YHU WKH FRXUVH RI WZR DQG D KDOI GD\V D WRWDO RI  EHUULHV ZHUH RIIHUHG ZLWKLQ WKH ZRRG WKUXVK H[KLELW  EHUULHV ZLWKLQ WKH KHUPLW WKUXVK FDJH DQG  EHUULHV WR WKH YHHU\ DQG 6ZDLQVRQ¶V WKUXVK$OO WKUXVKHV LQJHVWHG DW OHDVW  EHUU\ ZLWK WKH ZRRG WKUXVK LQJHVWLQJ WKH KLJKHVW QXPEHU RI EHUULHV RYHU WKH FRXUVH RI WZR DQG D KDOI GD\V ,QJHVWHG VHHGV ZHUH UHJXUJLWDWHG E\ DOO WKUXVKHV ZLWK DQ DYHUDJHWLPHRIPLQV“PLQVn = 9) between ingestion and regurgitation. The wood thrush ingested a total of 12 berries. Seven wood thrush regurgitation events ZHUH REVHUYHG ZLWK  HYHQWV RFFXUULQJ DIWHU D VSHFLILF and isolated feeding event. Of these isolated regurgitaWLRQHYHQWVDPHDQWLPHRIPLQV“PLQVZLWK D PLQLPXP WLPH RI  PLQ DQG D PD[LPXP RI  PLQ between ingestion and regurgitation was observed. 

7KH YHHU\ LQJHVWHG RQO\  EHUULHV ERWK RQHVHHGHG DQG KDGDPHDQWLPHRIPLQV“PLQVEHWZHHQLQJHVtion and regurgitation. The Swainson’s thrush ingested a VLQJOH WZRVHHGHG EHUU\ GXULQJ WKH VWXG\ DQG UHJXUJLWDWHG WKHILUVWVHHGPLQVDIWHULQJHVWLRQDQGWKHVHFRQGVHHG PLQVDIWHULQJHVWLRQ7KHKHUPLWWKUXVKGLGHDWEHUU\ RYHUWKHFRXUVHRIWKHVWXG\EXWWKHWLPHXQWLOUHJXUJLWDWLRQ was not recorded. However, given that the seed of the misVLQJEHUU\ZDVUHFRYHUHGFOHDQRISXOSDQGZLWKRXWIHFHV it was determined that a regurgitation event had occurred. $WRWDORIVHHGVWKDWKDGEHHQUHJXUJLWDWHGZHUHUHFRYHUHG ZRRGWKUXVK6ZDLQVRQ¶VDQGYHHU\KHUPLWWKUXVK  $OOUHFRYHUHGVHHGVZHUHIRXQGWREHYLDEOHE\WKHWHWUD]ROium test after regurgitation. Other bird species within the Delta exhibit at the Tennessee Aquarium ingested ginseng berries. Of the  EHUULHV RIIHUHG ZLWKLQ WKH H[KLELW FDUGLQDOV Cardinalis cardinalis) ate 47 berries, a summer tanager (Piranga rubra) ate 4 berries, and a cedar waxwing (Bombycilla cedrorum), a brown thrasher (Toxostoma rufum), and an orchard oriole (Icterus spurius  HDFK DWH  EHUU\ :KLOH most of the other species that ate berries were not observed for their digestive behaviours, the cardinals predated the JLQVHQJVHHGE\UHPRYLQJWKHSXOSDQGVHHGFRDWIURPWKH ginseng seed and ingesting the unprotected interior of the VHHGFRQWDLQLQJWKHSODQWHPEU\R

Before interpreting camera-trap results, it is importDQW WR DGGUHVV SRVVLEOH ELDV GXH WR WKH WHFKQRORJ\ LWVHOI Previous work with infrared, motion-activated wildlife FDPHUDVKDVVKRZQWKDWWKHUHLVXQFHUWDLQW\DVWRZKDWWULJJHUVDQHYHQWQRWRQO\EHWZHHQGLIIHUHQWPRGHOVRIFDPHUDV but also between individual cameras of the same model (Swann et al.  +XJKVRQ 'DUE\  'XQJDQ   :KLOH ZH WULHG WR GHFUHDVH WKLV XQFHUWDLQW\ E\ PRXQWLQJ FDPHUDV LQ D V\VWHPDWLF IDVKLRQ D QXPEHU RI HYHQWV WKDW WULJJHUHG WKH FDPHUDV GXULQJ WKLV VWXG\ GLG QRW UHVXOW in a visible potential disperser within the images. Three explanations for these uninformative images are possible:   WKH FDPHUD LV WULJJHUHG E\ VRPHWKLQJ RWKHU WKDQ DQ DQLPDO WKHFDPHUDLVWULJJHUHGE\DSRWHQWLDOGLVSHUVHUWKDW is out of frame or is hidden at the time of shutter release and therefore is not in the image (Swann et al.   RU  WKHFDPHUDLVWULJJHUHGE\DSRWHQWLDOGLVSHUVHUEXWYHU\ HIIHFWLYHFDPRXIODJHUHVXOWVLQWKHREVHUYHUIDOVHO\FRQFOXGLQJWKDWQRDQLPDOLVSUHVHQW)DOVHWULJJHUVPD\RFFXUGXH to environmental factors, such as the wind moving either vegetation or the camera mount (Swann et al.   7KLV cause would not bias the potential disperser information REWDLQHG E\ WKH FDPHUD EXW WKH RWKHU  FDXVHV FRXOG ELDV the set of images obtained in favour of slower moving, ODUJHU RU PRUH YLVLEOH DQLPDOV %\ VHWWLQJ WKH FDPHUDV WR WDNHLPDJHVSHUHYHQWWKHVHHUURUVFDQEHUHGXFHGLQIUHTXHQF\ DW WKH DQDO\VLV VWDJH E\ FDUHIXOO\ WRJJOLQJ EHWZHHQ the images to detect movement within the event. :KLOHDQXQNQRZQELDVLQWKHIUHTXHQF\RIFDSWXUHRI GLIIHUHQW VSHFLHV PD\ KDYH RFFXUUHG WKHVH FDPHUDV QHYHUWKHOHVV SURYLGH D VLPSOH DQG VRSKLVWLFDWHG PHWKRGRORJ\

ÉCOSCIENCE, VOL. 21 (1), 2014

a)

b)

c)

d)

FIGURE  D  ,PDJH RI DQ (DVWHUQ FKLSPXQN GHPRQVWUDWLQJ +LJK /HYHO LQWHUDFWLRQ EHKDYLRXU E\ WRXFKLQJ WKH JLQVHQJ LQIUXFWHVFHQFH E  ,PDJH RI D ZRRG WKUXVK GHPRQVWUDWLQJ +LJK /HYHO LQWHUDFWLRQ EHKDYLRXU ZLWK D EHUU\ LQ LWV EHDN F  ,PDJH RI D KHUPLW WKUXVK GHPRQVWUDWLQJ +LJK /HYHO LQWHUDFWLRQ EHKDYLRXUZLWKDEHUU\LQLWVEHDNG ,PDJHRID6ZDLQVRQ¶VWKUXVKGHPRQVWUDWLQJ+LJK/HYHOLQWHUDFWLRQEHKDYLRXUZLWKDEHUU\LQLWVEHDN

for observing plant–animal interactions that would be LPSRVVLEOH E\ GLUHFW REVHUYDWLRQ %\ XVLQJ ZLOGOLIH FDPHUDV D WRWDO RI  K  FDPHUDGD\V  RI REVHUYDWLRQ time were logged, resulting in sequences of images that ZHUH WKHQ DQDO\]HG FDUHIXOO\ LQ D ODE VHWWLQJ$GGLWLRQDOO\ wildlife cameras are less intrusive than human observers, ZKLFKFDQVWUHVVZLOGOLIHDQGGHFUHDVHWKHSUREDELOLW\RIDQ animal–ginseng interaction (Cutler & Swann, 1999). 8VLQJ ZLOGOLIH FDPHUDV WR REVHUYH DQLPDO LQWHUDFWLRQV with American ginseng, we have determined that animal– JLQVHQJ LQWHUDFWLRQV DUH YDULDEOH LQ LQWHQVLW\ DQG QRW DV UDUH DV SUHYLRXVO\ WKRXJKW )LYH SHUFHQW RI DOO HYHQWV ZLWK potential dispersers were categorized as High Level interDFWLRQV :KLOH WKHVH GLG QRW RFFXU DW HYHU\ FDPHUD ORFDWLRQ WKH\ UHVXOWHG LQ UHPRYDO RI DOO RI WKH EHUULHV IURP DQ infructescence at 1 of the camera locations (Table III). Of WKH SRWHQWLDO GLVSHUVHUV REVHUYHG WKUXVKHV SDUWLFXODUO\ ZRRG WKUXVKHV PRVW IUHTXHQWO\ UHPRYHG EHUULHV GLUHFWO\ from the plants, but chipmunks also had High Level interDFWLRQV ZLWK JLQVHQJ LQIUXFWHVFHQFHV$GGLWLRQDOO\ LQWHUDFWLRQVFDWHJRUL]HGDV/HYHOLQWKH/RZ/HYHOLQWHUDFWLRQV GHPRQVWUDWHIRUDJLQJEHORZWKHJLQVHQJSODQWVWKHVHHYHQWV PD\ KDYH UHVXOWHG LQ VHFRQGDU\ GLVSHUVDO E\ VPDOO PDPPDOV 9DQGHU :DOO .XKQ  *ZRUHN  9DQGHU :DOO  %HFN   0DQ\ SHUHQQLDO XQGHUVWRU\ KHUEV VXFK DV

ginseng do not produce large crops or large seeds, which PD\ PDNH WKHP D ORZ SUHIHUHQFH LWHP IRU VPDOO PDPPDOV LQFUHDVLQJ WKH VHHGV¶ SUREDELOLW\ RI VXUYLYDO DIWHU EHLQJ FDFKHG %DUJD  9DQGHU :DOO   +RZHYHU VPDOO PDPPDO±VHHG LQWHUDFWLRQV FDQ EH KLJKO\ YDULDEOH and, in the case of small seeds, can result in seed predation events, which could contribute to ginseng population decline (e.g. )HQQHU  9DQGHU :DOO  5XVFK 0LGJOH\ $QGHUVRQ   +LJK /HYHO WKUXVK±JLQVHQJ LQWHUDFWLRQV DUH PRVW IUHTXHQWO\ UHSUHVHQWHG LQ WKH GDWD PDNLQJ WKUXVKHV WKH PRVW OLNHO\ FDQGLGDWH IRU DQLPDO GLVSHUVDOHYHQWVEH\RQGWKHGLVWDQFHVUHFRUGHGIRUGLVSHUVDOE\ JUDYLW\9DQGHU9RRUW  :RRGWKUXVKHVPD\KDYHEHHQWKHPRVWFRPPRQDYLDQ species to trigger an event because their breeding habiWDW UDQJH LV QHDUO\ LGHQWLFDO WR WKDW RI$PHULFDQ JLQVHQJ 6LEOH\   +HUPLW WKUXVKHV DQG 6ZDLQVRQ¶V WKUXVKHV the other 2 thrush species to have High Level interactions, KDYH D PRUH QRUWKHUQ EUHHGLQJ UDQJH DQG PD\ EH PRUH OLNHO\ WR LQWHUDFW ZLWK JLQVHQJ LQ WKH QRUWKHUQ SRUWLRQ RI JLQVHQJ¶V UDQJH 6LEOH\  $GGLWLRQDOO\ WKH YHHU\ D species that was not observed on camera but was fed durLQJ WKH FDSWLYH IHHGLQJ WULDOV PD\ QRW KDYH EHHQ GHWHFWHG during field observations because their breeding range 

HRUSKA, SOUTHER & MCGRAW: SONGBIRD DISPERSAL OF AMERICAN GINSENG

LLI

HLI 1 Wood thrush

0.9

Hermit thrush

0.8

Ovenbird

Swainson's thrush

0.7

0.6 Proportion of events

Northern cardinal Wood thrush

0.5

Turkey

0.4

Tufted titmouse

0.3

0.2

American robin

0.1

Eastern towhee

Hermit thrush Crow

Unidentified thrush 0

0

5

10

15

20

25

30

Thrushes

35

40 Not thrushes

45

Number of events F IGURE  3DUWLWLRQLQJ RI WKUXVK DQG QRQWKUXVK SRWHQWLDO GLVSHUVHU HYHQWV EDVHG RQ FDWHJRULHV WKDW ZRXOG OHDVW OLNHO\ UHVXOW LQ D GLVSHUVDO HYHQW//,/RZ/HYHORI,QWHUDFWLRQ DQGPRVWOLNHO\UHVXOWLQDGLVSHUVDOHYHQW+/,+LJK/HYHORI,QWHUDFWLRQ ZLWKWKHSURSRUWLRQRIVSHFLHVZLWKLQ HDFKFDWHJRU\

EDUHO\ RYHUODSV the northern portion of the region where ZLOGOLIH FDPHUDV ZHUH SODFHG 6LEOH\   %XW WKH\ WRR could ingest ginseng pre-migration and at stopover sites en route to their wintering grounds. Our feeding studies demonstrated that after berries ZHUH LQJHVWHG E\ D WKUXVK VSHFLHV YLDEOH JLQVHQJ VHHGV ZHUHUHJXUJLWDWHG0H\HUDQG:LWPHU GHPRQVWUDWHG that the germination of similar seeds with similar germination requirements (spicebush: Lindera benzoinDUURZZRRG viburnum: Viburnum dentatum FKRNHFKHUU\ Prunus virginiana  ZHUH QRW DIIHFWHG E\ WKUXVK UHJXUJLWDWLRQ ZKHQ grown in a controlled greenhouse setting. Given that ginseng has a high natural germination rate in the field (gerPLQDWLRQSUREDELOLWLHVDVKLJKDVLQWKHILHOGUHYLHZHG in McGraw et al.   LI JHUPLQDWLRQ LV QRW KLQGHUHG E\ WKUXVK UHJXUJLWDWLRQ WKHUH LV D KLJK SUREDELOLW\ WKDW VHHGV GLVSHUVHGE\WKUXVKHVZLOOJHUPLQDWHDQGSHUVLVWZKHQGLVpersed to a suitable site. The distances traveled between ingestion and regurgitation sites are expected to be shorter than distances traveled 

between ingestion and defecation sites, given the amount RIWLPHWKHVHHGVVWD\ZLWKLQDELUG¶VGLJHVWLYHV\VWHPe.g., 0H\HU  :LWPHU  &ODUN et al.  8ULDUWH et al.,   2Q DYHUDJH JLQVHQJ VHHGV ZHUH UHJXUJLWDWHG DIWHU 16 min, which is consistent with other recorded thrush regurgitation times for seeds of similar sizes (L. benzoin, V. dentatum, P. virginiana0H\HU :LWPHU  &RQWUDVWLQJ EHKDYLRXUV H[KLELWHG E\ DGXOWV DQG MXYHQLOHV GXULQJ WKH VHHG GLVSHUVDO VHDVRQ PD\ UHVXOW LQ GLIIHUent sets of dispersal distances for ingested ginseng seeds. 3RVWEUHHGLQJ DGXOW ZRRG WKUXVKHV UHORFDWH ± P from nesting sites to new molting sites (Vega Rivera et al.,   :KLOH WKHVH GLVWDQFHV PD\ QRW EH WUDYHUVHG ZLWKLQ  IOLJKW WKH\ GR WHQG WR RFFXU GXULQJ ODWH -XO\ DQG HDUO\ $XJXVW DQG FDQ RYHUODS ZLWK WKH HDUO\ ULSHQLQJ RI JLQVHQJ berries (Vega Rivera et al. E 0F*UDZ et al.   However, once adult thrushes begin their pre-migration molt, which is centred on the ginseng seed ripening period, WKHLUDELOLW\WRIO\LVGUDVWLFDOO\UHGXFHG7KLVFDXVHVWKHPWR become secretive and find areas of dense forest cover and

ÉCOSCIENCE, VOL. 21 (1), 2014

high food abundance in order to avoid predator detection (Vega Rivera et al.E 'XULQJWKHLUPROWDGXOWWKUXVK PRELOLW\ GHFUHDVHV E\ DOPRVW  FRPSDUHG WR PRYHPHQW during breeding season (Vega Rivera et al., 1999), sugJHVWLQJWKDWDGXOWWKUXVKHVZLOOPRVWOLNHO\PRYHVHHGVOHVV WKDQPEHWZHHQLQJHVWLRQDQGUHJXUJLWDWLRQVLWHVGXULQJ their molt. Smith et al.   REVHUYHG D  SUREDELOLW\ WKDW D KHUPLW WKUXVK ZLOO GLVSHUVH D VHHG OHVV WKDQ  P IURPWKHLQJHVWLRQVLWHRYHUDPLQWLPHSHULRGGXULQJWKH ZLQWHU VHDVRQ EXW WKLV GLVWDQFH PD\ XQGHUHVWLPDWH KHUPLW thrush movement during the fall because hermit thrushes DUHSULPDULO\WHUULWRULDORQWKHLUZLQWHULQJJURXQGV%URZQ 6WURQJ 6WRXIIHU  Juvenile thrushes, however, undergo a pre-basic molt prior to migration and spend time searching for optiPDO IRUDJLQJ VLWHV DQG PDNLQJ H[SORUDWRU\ PRYHPHQWV (Vega Rivera et al. D  ZKHQ JLQVHQJ EHUULHV DUH ULSH (McGraw et al.  $IWHU OHDYLQJ WKH QDWDO VLWH \RXQJ WKUXVKHV ZLOO WUDYHO  P RQ DYHUDJH WR D GLVSHUVDO VLWH DQG ZLOO WUDYHO WR DV PDQ\ DV  GLIIHUHQW GLVSHUVDO VLWHV before their migration (Vega Rivera et al. D  :LWKLQ WKHVH GLVSHUVDO VLWHV MXYHQLOHV PRYH DSSUR[LPDWHO\  P EHWZHHQ FRQVHFXWLYH ORFDWLRQV DQG RFFDVLRQDOO\ PDNH H[SORUDWRU\ PRYHPHQWV JUHDWHU WKDQ  P IURP WKH GLVpersal site (Vega Rivera et al. D  7KH ODUJHU UDQJH RI PRELOLW\ RI MXYHQLOH WKUXVKHV SURYLGHV DQ RSSRUWXQLW\ IRU UDSLGVHHGGLVSHUVDOEH\RQGP 9HU\ ORQJ GLVWDQFH GLVSHUVDO KXQGUHGV RI NLORPHWHUV  RI JLQVHQJ VHHGV E\ WKUXVKHV XQGHUWDNLQJ WKHLU DQQXDO PLJUDWLRQ ZLOO OLNHO\ EH UDUH ERWK EHFDXVH UHWHQWLRQ RI VHHGV LV UHODWLYHO\ VKRUWOLYHG DQG EHFDXVH WKH SUREDELOLW\ of ingesting a ginseng seed as the last meal prior to taking IOLJKW LV ORZ 'LVSHUVDO GXULQJ PLJUDWLRQ LV DOVR XQOLNHO\ to be effective as a mechanism for responding to climate change, since the direction of movement would be opposite to that which would enable populations to track their SUHIHUUHG WHPSHUDWXUH ]RQHV 6RXWKHU  0F*UDZ   1HYHUWKHOHVV PRYHPHQW RI VHHGV E\ WKUXVKHV RQ WKH RUGHU RI KXQGUHGV RI PHWHUV SDUWLFXODUO\ PRYHPHQW XS LQ HOHYDtion, could be important for tracking climate change. American ginseng is a species that was once abundant throughout Appalachian forest but is now located in thousands of small populations with a clustered spatial distriEXWLRQ &UXVH6DQGHUV  +DPULFN D 0F*UDZ et al.,  :KLOHVHHGGLVSHUVDOKDVEHHQSUHYLRXVO\FRQVLGHUHG WREHSULPDULO\YLDJUDYLW\DQGWKHUHIRUHOLPLWHGRXUILQGLQJV VWURQJO\ VXJJHVW WKDW GLVSHUVDO HYHQWV E\ WKUXVKHV are not rare. The variation of High Level thrush–ginseng interactions between camera locations from frequent to DEVHQWVXJJHVWVWKDWYDULDWLRQLQKDELWDWVXLWDELOLW\IRUSRVW breeding thrushes (Ozinga et al.  5XVVR 3RUWQR\  $XJVSXUJHU   ZLOO GHWHUPLQH WKH IUHTXHQF\ RI VXFK dispersal events. $PHULFDQ JLQVHQJ¶V EURDG QLFKH PD\ HQDEOH LW to persist in sites where thrush populations are low or QRQH[LVWHQW 3RSXODWLRQV LQ WKHVH VLWHV ZRXOG OLNHO\ EH confined to smaller areas and would tend to be found in  RU D IHZ LVRODWHG SDWFKHV UDWKHU WKDQ PDQ\ GLVSHUVHG

FOXVWHUV&UXVH6DQGHUV +DPULFND +RZHYHUJLQseng growing in habitats that provide an abundance of food UHVRXUFHVDQGSURWHFWLYHFRYHUZRXOGEHPRUHOLNHO\WRKDYH frequent interactions with thrushes and a greater probabilLW\ IRU GLVSHUVDO EH\RQG  P DV ZHOO DV IRU ORQJGLVWDQFH dispersal events in areas with a higher number of juvenile WKUXVKHV 'LVSHUVDO DFURVV WKH ODQGVFDSH E\ WKUXVKHV FRXOG SURGXFHQRWRQO\PDQ\QHZVXESRSXODWLRQVZLWKLQDSRSXlation, but also new populations across the landscape. Most demographic models for plants assume random disperser movements, but movement is most often the result of nonUDQGRP EHKDYLRXUV 6FKXSS -RUGDQR  *yPH]   ,Q RUGHU WR LQFRUSRUDWH WKHVH GDWD LQWR D VSDWLDOO\ H[SOLFLW demographic model for ginseng, research investigating the VSHFLILF W\SHV RI KDELWDWV ZKHUH ERWK WKUXVKHV DQG JLQVHQJ are present, their population densities, and their movement patterns on a minute time scale is needed. :LWK WKUXVKHV QRZ NQRZQ WR EH SULPDU\VHHG GLVSHUVHUV WKH UHFRYHU\ DQG FRQVHUYDWLRQ RI WKUXVK DQG JLQVHQJ populations in North America are connected. Thrush populations have been declining in North America since the late V GXH WR KDELWDW ORVV IUDJPHQWDWLRQ DQG GHJUDGDWLRQ e.g., acid rain and brown-headed cowbird parasitism (Trine,  +DPHV et al.  %HWWV et al.   *LQVHQJ SURvides a source of food for thrushes prior to migration, and thrush dispersal of ginseng seeds in turn could improve JLQVHQJ¶VUHVLOLHQFHLQWKHIDFHRIWKHPRVWLPSRUWDQWIDFtors shown to be causing population decline: deer browse, harvest, and climate change (McGraw et al. 7KUXVK GLVSHUVDO SURYLGHV WKH RSSRUWXQLW\ IRU JLQVHQJ WR EH GLVSHUVHGDZD\IURPDUHDVZLWKKHDY\GHHUWUDIILFDQGDUHDVRI intense foraging, which is important because, in addition to having negative effects as herbivores (McGraw & Furedi,   GHHU DUH VHHG SUHGDWRUV )XUHGL  0F*UDZ   6LPLODUO\ E\ SURYLGLQJ WKH RSSRUWXQLW\ IRU WKH HVWDEOLVKment of new populations, thrush dispersal also provides D ZD\ RI HVFDSLQJ KDUYHVW +DUYHVWHUV UHWXUQ \HDU DIWHU \HDU WR WKH VDPH JLQVHQJ SRSXODWLRQV 0F*UDZ 6RXWKHU  /XEEHUV   VR GLVSHUVDO DQG HVWDEOLVKPHQW RI QHZ populations in areas where ginseng no longer exists could mitigate the effect of harvest on ginseng metapopulations. )XUWKHUPRUH WKH DELOLW\ RI WKUXVKHV WR DFW DV D SULPDU\ GLVSHUVHU SURYLGHV WKH JUHDWHVW RSSRUWXQLW\ IRU JLQVHQJ WR persist the face of climate change effects. Longer dispersal movements via thrushes would provide a greater opporWXQLW\ IRU JHQH IORZ EHWZHHQ ORFDOO\ DGDSWHG SRSXODWLRQV 6RXWKHU  0F*UDZ  6RXWKHU  0F*UDZ   ZKLFKPD\LQWXUQHQKDQFHWKHDELOLW\RISRSXODWLRQVWRSHUsist in the face of climate change. Acknowledgements We would like to thank J. Chandler, M. Elza, and J. Turner for their help with camera set up, image collection, and aquarLXP REVHUYDWLRQV DQG WKHLU IHHGEDFN RQ WKH HDUO\ YHUVLRQ RI this article. We thank the Tennessee Aquarium for the use of their facilities and care of the birds, in particular A. George and . &DOKRRQ IRU DOO RI WKHLU DVVLVWDQFH )LQDQFLDO VXSSRUW ZDV received from National Science Foundation Long Term Research LQ(QYLURQPHQWDO%LRORJ\*UDQW'(%DQG'(% (to J. B. McGraw). 

HRUSKA, SOUTHER & MCGRAW: SONGBIRD DISPERSAL OF AMERICAN GINSENG

Literature cited $PHULFDQ2UQLWKRORJLVWV¶8QLRQ7KH&RGHRI1RPHQFODWXUH DQG &KHFN/LVW RI 1RUWK $PHULFDQ %LUGV $GRSWHG E\ WKH $PHULFDQ 2UQLWKRORJLVWV¶ 8QLRQ %HLQJ WKH 5HSRUW RI WKH &RPPLWWHH RI WKH 8QLRQ RQ &ODVVLILFDWLRQ DQG 1RPHQFODWXUH Forgotten Books, New York, New York. $XJVSXUJHU&.6HHGOLQJVXUYLYDORIWURSLFDOWUHHVSHFLHV Interactions of dispersal distance, light-gaps, and pathogens. (FRORJ\± %DUJD 6 &  6 % 9DQGHU :DOO  'LVSHUVDO RI DQ KHUEaceous perennial, Paeonia browniiE\VFDWWHUKRDUGLQJURGHQWV eFRVFLHQFH± %DVNLQ & &  - 0 %DVNLQ  6HHGV (FRORJ\ %LRJHRJUDSK\ DQG (YROXWLRQ RI 'RUPDQF\ DQG *HUPLQDWLRQ Academic Press, San Diego, California. Betts, M. G., J. C. Hagar, J. W. Rivers, J. D. Alexander, . 0F*DULJDO  % & 0F&RPE  7KUHVKROGV LQ IRUHVW ELUG RFFXUUHQFH DV D IXQFWLRQ RI WKH DPRXQW RI HDUO\VHUDO broadleaf forest at landscape scales. Ecological Applications, ± %URZQ ' 5 & 6 6WURQJ  3 & 6WRXIIHU  0RYHPHQW DQG WHUULWRULDOLW\ RI ZLQWHULQJ +HUPLW 7KUXVK LQ VRXWKHDVWHUQ /RXLVLDQD:LOVRQ%XOOHWLQ± Clark, C. J., J. R. Poulsen, B. M. Bolker, E. F. Connor & 9 7 3DUNHU  &RPSDUDWLYH VHHG VKDGRZV RI ELUG PRQNH\DQGZLQGGLVSHUVHGWUHHV(FRORJ\± &ODUN&--53RXOVHQ'-/HYH\ &:2VHQEXHUJ Are plant populations seed limited? A critique and metaDQDO\VLV RI VHHG DGGLWLRQ H[SHULPHQWV$PHULFDQ 1DWXUDOLVW ± &ODUN' '&ODUN6SDFLQJG\QDPLFVRIDWURSLFDOUDLQforest tree: Evaluation of the Janzen–Connell model. American 1DWXUDOLVW± &RXVHQV 5 & '\WKDP  5 /DZ  'LVSHUVDO LQ 3ODQWV $3RSXODWLRQ3HUVSHFWLYH2[IRUG8QLYHUVLW\3UHVV2[IRUG &UXVH6DQGHUV-0 -/+DPULFND6SDWLDODQGJHQHWLF structure within populations of wild American ginseng (Panax quinquefolius/$UDOLDFHDH -RXUQDORI+HUHGLW\± &UXVH6DQGHUV-0 -/+DPULFNE*HQHWLFGLYHUVLW\LQ harvested and protected populations of wild American ginseng, Panax quinquefolius L. (Araliaceae). American Journal of %RWDQ\± &XWOHU 7 /  ' ( 6ZDQQ  8VLQJ UHPRWH SKRWRJUDSK\ LQ ZLOGOLIH HFRORJ\ $ UHYLHZ :LOGOLIH 6RFLHW\ %XOOHWLQ ± 'LYLVLRQ RI 0DQDJHPHQW $XWKRULW\  86 H[SRUWV RI $PHULFDQ JLQVHQJ ± 86 )LVK DQG :LOGOLIH 6HUYLFH Department of the Interior, Washington, DC. (QJOHU 5 $ *XLVDQ  0LJ&OLP 3UHGLFWLQJ SODQW GLVWULEXWLRQ DQG GLVSHUVDO LQ D FKDQJLQJ FOLPDWH 'LYHUVLW\ DQG 'LVWULEXWLRQ± )HQQHU 0 HG   6HHGV 7KH (FRORJ\ RI 5HJHQHUDWLRQ in Plant Communities. 2 nd Edition. CAB International, Wallingford. )XUHGL 0 $  - % 0F*UDZ  :KLWHWDLOHG GHHU Dispersers or predators of American ginseng seeds? American 1DWXUDOLVW± +DFNQH\ (  - % 0F*UDZ  ([SHULPHQWDO GHPRQVWUDWLRQ RIDQ$OOHHHIIHFWLQ$PHULFDQJLQVHQJ&RQVHUYDWLRQ%LRORJ\ ± 

+DPHV 5 6 . 9 5RVHQEXUJ - ' /RZH 6 ( %DUNHU  $$ 'KRQGW $GYHUVH HIIHFWV RI DFLG UDLQ RQ WKH GLVtribution of the wood thrush Hylocichla mustelina in North $PHULFD 3URFHHGLQJV RI WKH 1DWLRQDO$FDGHP\ RI 6FLHQFHV ± +RZH + )  - 6PDOOZRRG  (FRORJ\ RI VHHG GLVSHUVDO $QQXDO5HYLHZRI(FRORJ\DQG6\VWHPDWLFV± +XJKVRQ'/1:'DUE\ -''XQJDQ&RPSDULVRQ of motion-activated cameras for wildlife investigations. &DOLIRUQLD)LVKDQG*DPH± ,OX] '  =RRFKRU\ 7KH GLVSHUVDO RI SODQWV E\ DQLPDOV 3DJHV ± LQ - 6HFN  = 'XELQVN\ HGV $OO )OHVK LV Grass: Plant–Animal Interrelationships. Springer, Dordrecht. ,]KDNL, 816DIULHO:K\DUHWKHUHVRIHZH[FOXVLYHO\ IUXJLYRURXV ELUGV" ([SHULPHQWV RQ IUXLW GLJHVWLELOLW\ 2LNRV ± -RKDQQVHQ .  *LQVHQJ 'UHDPV 7KH 6HFUHW :RUOG RI $PHULFD¶V0RVW9DOXDEOH3ODQW8QLYHUVLW\3UHVVRI.HQWXFN\ /H[LQJWRQ.HQWXFN\ -RUGDQR 3 $YLDQ IUXLW UHPRYDO (IIHFWV RI IUXLW YDULDWLRQ FURSVL]HDQGLQVHFWGDPDJH(FRORJ\± .DUWH] - 7 $ 6\QRQ\PL]HG &KHFNOLVW RI WKH 9DVFXODU )ORUDRIWKH8QLWHG6WDWHV&DQDGDDQG*UHHQODQGnd Edition. Timber Press, Portland, Oregon. /DPEHUW)53LJHRQVDVVHHGSUHGDWRUVDQGGLVSHUVHUVRI ILJVLQ0DOD\VLDQORZODQGIRUHVW,ELV± /HYH\ ' -  6HHG VL]H DQG IUXLWKDQGOLQJ WHFKQLTXHV RI DYLDQIUXJLYRUHV$PHULFDQ1DWXUDOLVW± /HZLV: + 9 ( =HQJHU  '\QDPLFV RI$PHULFDQ JLQseng Panax quinquefolium (Araliaceae). American Journal of %RWDQ\± 0F*UDZ - %  0 $ )XUHGL  'HHU EURZVLQJ DQG SRSXODWLRQ YLDELOLW\ RI D IRUHVW XQGHUVWRU\ SODQW 6FLHQFH ± 0F*UDZ - % 6 0 6DQGHUV  0 ( 9DQ GHU 9RRUW  Distribution and abundance of Hydrastis canadensis L. (Ranunculaceae) and Panax quinquefolius L. (Araliaceae) in FHQWUDO$SSDODFKLDQ UHJLRQ -RXUQDO RI WKH 7RUUH\ %RWDQLFDO 6RFLHW\± 0F*UDZ - % 6 6RXWKHU $ ( /XEEHUV  5DWHV RI KDUvest and compliance with regulations in natural populations of American ginseng (Panax quinquefolius L.). Natural Areas -RXUQDO± 0F*UDZ-%0$)XUHGL.0DLHUV&&DUUROO*.DXIIPDQ A. Lubbers, J. Wolf, R. C. Anderson, M. R. Anderson, B. Wilcox, D. Drees, M. E. Van der Voort, M. A. Albrecht, $ 1DXOW + 0DF&XOORFK $ *LEEV  %HUU\ ULSHQLQJ and harvest season in wild American ginseng. Northeastern 1DWXUDOLVW± 0F*UDZ - %$ ( /XEEHUV 09DQ GHU9RRUW ( + 0RRQH\ 0$ )XUHGL 6 6RXWKHU - % 7XUQHU  - &KDQGOHU  (FRORJ\ DQG FRQVHUYDWLRQ RI JLQVHQJ Panax quinquefolius) LQ D FKDQJLQJ ZRUOG$QQDOV RI WKH 1HZ