Theory and its Application in a Changing World

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Theory and its Application in a Changing World

Edited by

Andrew J. Dennis Eugene W. Schupp Ronda J. Green

and

David A. Westcott

Rainforest C RC

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+

¹⁶¹7 395 4056

Fdh:

+

1 51 7 354 l i H i R F-mall: cahi-nao@cabt otx

0 CAB Intei-rlalio~~al 20[17. 2211 1-ights rescrvrtl. N o pal-t orthis pu1)lication may be I-cl>j,ortuced in any f i w n 01. ly any means, elettro~iirally. ~nechanically. b!

pliotnrrrpyrng, rec.ordi11g ur utlrcl-wisc:. withotrt the pt-iur p~smirsion nf the copyl.ight owners.

A c ~ t a l u ~ u c I-ccnrrl fr~r this book i s ;~vailable from the Britis11 I-ihrary, London. L'K.

Library of Congress Cataloging-in-Pubtimtirm Dam Sccd diqpersal : theriry rid its :ipplicatio11 111 ;z changing ~rrorld / edrrud by Anrll-ew,J. Ilennis ... [@l crl.1.

p. cm.

Includes hihlici~laphical references and lntlcx.

ISHN 978-1-3,1593- 165-0 (aik. paper)

l . Se~r~c--nirp~rsal--C;ongre5b~s, 1 nennis, Andrew J , H. Title.

QK!)%!IS443 2007 581.4 '67--tlc2:!

9007002294

Prodt~ced .~nrl r?.prac[ 1,). Co1uln11s D e \ l ~ t ~ I.td, Keading. U K Prit>red ancl hound In ~ h c U1: h~ B~dcllrs Ltd. Kjng's 1-ynn

Contributors ^IX

Preface X 1'

PART I Frugivores and Frurugivnry A

,l.

D P T ~ ~ I ! ~

I Seed Allornetry and Disperser Assemblages in Tlopical

Rainforests: h Comparison of Four Floras o n Different Conrincnts 5

! : - J f . fi)~g~l, A , [ D ~ T L I $ , X J 1\fazf7. I'A. . J O J I W I ! , S. hit(irn?~iu.

J E. Lnrt~hrri nrtd D.A. It>rrroll

2 Evolutionary Ecology OF Secondary Compounds in Ripe Fruit:

Gaze Studies with Capsaicin and Emodin S7

D.[.

I.r,~e+t, jJ.J 'li,rllk</nr~lr. I. Izitnkr, I:' 7;nhor r ~ d

D

I:. l l m k

3 The Evolutian of Visual Fruit Signals: Concepts and Constraints 5') H.IIJI. S r h o ~ ( ~ l . onrl I! S C ~ ( I P { Y T

4 A Review on the Role of Endozoochory in Seed Germination i H A . 7jr~1zl~srt, A . 11' Rohu~tson orid.]. R r ~ E r i f l r r - P ~ T P Y

5 Living in the Land o f Ghosts: Fruit Traits and the Importance of Large Mammals as Geed Dispersers in the Pantanal, Brazil 1 IbI (:.I. L)onul!f, IIJ CalptEi. 11.I.1I. Pz20, P R . C Z I Z J I I I I I ~ E T J r ~ n d I? Judrrnt~

6 The Importance of Lizards as Erugivores and Seed Dispersers 12-1 rl. 1$ii1d0 clndJ.~Zi. O / P ~ P ~

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Role of Endozoochoty in Seed Germination 79

4 ^{A Review} ^on ^{the Role} ^of

Endozoochory in Seed Germination

b. TRAVESET, A.W. ROBERTSON ^AND J . RODR~GUEZ-P~REZ

Introduction

A l n ~ g e fraction d l i v i n g plnt~ts pmrlucr fi-llits that attract a~limals (W7c anrl 27% ol- gyrrlllosperm a n d angiospctln lineagcs, respcctirely; tlerrera ancl Pellttlyl: 20112). In ronsuming rheln. nnimals can spi-ead the sccds to more or less C { ~ S ~ I E ~ sites Tram the parent plant, Lhus cr~ntributi~lg to plant rrge~lerntion and colur~izatiori

or

new sites ^(IVilIuona n d Traveset, 2000, anrl I-clcrences therein). Fui- nlilliuns or p;~r-S both the pulp and seeds of fruit have been suhjrc~ecl to selccrivt: pressuies exerled by fr~~givorcs arlcl granivorcs. F1,uit consumers, specifically. may sl-iow preferet~ccs fur fiwit traits siicki as size, shapc, chernical cornposirinn nnrl others, nncl Ilavc specific morphologies and p l ~ ~ s i o l o g ~ e s (IT the digtstive tract that a f k t l the survival probability of rlw ingcstecl secrls in diflercnt ways (Hrrrcia atiri Pe111nr.r~ 2002, atlcl rrfcrcnces therein). Seed traits arc unclcr fui-ther selective pressrires imposed 11); a nuintlcr of biotic (antagnniatic fungi, insects ancl microhcc; Lipollini ancl Lcvey. 1997) and a'tliotic factors (e.g.

light, temper;lt urc. I-ainkill: Holl, 1999; I,eishmar~ rl al., 2000) that inflriencr tile dornlat~cy gcrminatinn timr andlol- f ~ ~ t u r e seedling growth, which can llltimately determine get-mi~latiorl and seedling success (Vcrclil ancl 7i-avcset, 2005, and rdertr~ct.s thereill). T~liercfore, the specilic seecl

~ r a i t s irl a n endozoocllart>tls plant are a result uf 111c combinetl selectir>n irnposeerl hy frugiv~trcs, .I-anivor-es ancl other hioric i l r ~ r l abiotic Bctors.

In th~n cl~aptel; we ev:lluate tltt. role oC rndu-roorhnry nn seed

~ e r ~ ~ ~ i n a t i u n . We I-cview the i11rorm;ition gatherecl on gcrminarien patterns itr rxperilnrnts aimed at e s a m i n i t ~ g the elycct of a sced's passage through a rri~~ivni-e's gut, i ~ n d give Lilrthrr rlircctiuns on metfiocls for l u t ~ t r c stutlirs.

FI-nil treatimcnt in thc disperser's tli~estive tract (which includes pulp separatior~ from scerls and trentmrnt o f the seeds) can determine the capacity of sccds trr gel-mjnare and, thus, is one o f the mlnpoilents nt'

rliuperscr rffective~~ess that t i ~ i ~ y ljc cruckil Tn1- h e populatir~rl rlyna~nics of many Rel;hir-fruited plant spccies. The ri~tilre n l ' t l ~ r relationship.; I~el~vccn fruit c h r r ~ n i s t r ~ and moi-pt~ology ancl tIir typc of- clisperser. is crucial to

unders~aildillg thr co-evolutivn of- plant-r~-~~girore intrl-actinns ( C . $

Murl-ay c! 01.. 1994; Cipnilini and I.evY!,, 1995; \2::1h;?i ^P!d., 1991;: K e p n rt d., 200 1: 'I'P~cksbnry and Nabl~an, 200 l ; \IJcnny, 200 1 : S~anlcy and I-ill.

20Cl2b: Aldntara allcl Re?, 2I103).

Biology

of the

System: From

Fruit

SwaElowing

to

Seed

Fate Frugivorcs that slvallow fruits (subsequrntly rcicri-ecl t u as rr~~givares) acr differentially un secds in sevei-al r\.ays during itigestion, gut-processing and drferatiol~. Hants, it1 ttrrn, can be expcctcd to crcdve physical and clle~llical adaptaticlns in l i d s anrl sccds to clirec~ dispersal ant1 to maximrrc 1 1 1 r b

proportion of scecls that ai-e s~rcccssfully riispersccl and r ~ t a l ~ l i s h c ~ l [Table 4.1). f3elo1v we briefly nutline the is~ucs surruu~irling four main conlporlcllts of the process and Follow this with det:kiletl revicws in each ayca.

Removal of putp surrounding the seed@)

Fruit pulp oftcn contains germination ir~hrllitors that can I~lrlck blocheniical pathwars of germination (e.g. Uvcnai I, 1941;1, Maycr and Pr~ljakofT-Mm her.

1982; Clpollini and Level, 10117, and references tlicre~n; \fryer and \Vtrm?r, 1998). Irlarrcrves, the pulp can cl~rrcase and even prcclude genr~itiar~on l>!

Table 4.1. Aspects of fruit processing durlng endozoochorj likely to Influence the qermination of seeds when they are subsequently depos~ted.

Pulp removal Gut passage Frugrvore All frugivores adequate Large frug~vores, attributes except fruit peckers. espec~ally mammals,

have lengthy passage tlmes and are chem~cally and mechantcally harsh.

Birds tend to be more gentle and pass seeds faster.

Djei may ^have important effects.

Depos~tion pattern Rsgurgrtators tend to dmp seeds s~ngly but often close to the maternal tree.

Large defecators produce dung w ~ t h large numbers ol seeds and hrgh rates of seed rnrxlng

Small frug~vores deposit smallnumbers

seed-mixing. of seeds wlth less Fru~t Many plants appear to Passage rates may be Seeds may contarn

chemrstry have germination influenced ^bysecondary allelochem~cals that inh~bit the lnh~bdors In Ihe putp that metabolites that act elther germination of compet~tors must be removed before as laxat~ves or with~n the same faecal clump gemlnatlon will occur. constipating agents

Q CAB International 2007. Seed Dispersal: Theory and rtsqoplication in a Changing World ( ~ d s A.J. Denn~s et al.)

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Rote of Enduz~ochoty in Seed Germination R1

80 A. Traveset et al.

altcring tllc seerls' iiiiuroc~~vil-onirle~x (e.g. uutllotir prcssurt. ancl light reginw: >,f;rycr allcl l'nlj:~koE-kJa~-i~er~ hjej-er xnri \,\'it~tles. l<VlS:

S;mli~els anil Lcvry. 2UIE5). -I'11r rrlnr>val ot' fi-uit pulf) ant1 conscquenl relleast:

rrf-rlie sced 1'1-urn this kincl of i n h j l ~ t i c l ~ ~ (tlie rlrit~hihlrior~ e R c t

-

Rnht.rtson rl irl., 2llOfi) has not I-ereirccl as rrlucl~ attcntion as scal-ilication (tlw ~nrt:hanrci~l a11d clle~nical processing of tIic scccl cryat or endocarp). l)t~t tlir filet that secds

; ~ l - c ninre (11. less Frfccl r , f pulp ill thr ti-~~gicol-e's jiut i s pnrt of the srcd p;~s.;agc 111-"less ant1 thus nt.rr2~ tu bc consi(lercd in luture sturlier, rspccially rr.hr11 rile f;~te nt tlitcntt.11 tj- tit^. i s ~,~,trsirlcl.ed (Sanl~lr-Is ant2 Leve!, "003;

Kohri-I ';on r t (I!. , 1200(i).

Mechanical andlor chemlcal scarification of the seed coat or endocarp T h t rffcct ol'scarificat ion 1s u\i~all? t l ~ o u g l ~ t to rlcprnd on rctet~tion t ilnc in

tllc drgeqtivc t~.lct ancl o n the type of rood i~rgcsted along wlrh \reds (Rarnea pt a / , 1990; %avcset. 1995). T h ~ s mechanisln (ratller tIiatl ctrirlllib!t~c>n) i s t h y tt~ost often invoked when cornpirtrng srrrl gernlInatlon parrerns \)rtrvcen ingestetl ancl uni~lgesterl setrls of the same cpecler (Sarnucls a i d Lcvey. 'lOO5). Drspite t l l i ~ . we have vei?' Ilttle dii ^ecteni~~il.ical cvidrt>ce of w c h a l t c ~ ~ ~ r i o n of t l ~ c scerl coat or. e n d o c a ~ p s t r i i c t ~ ~ r ~

Effect of the faecal material In which seeds are embedded at the time of deposition

Tlic residue\ 01- whatever Sr~od items a frl~givore has hcen rating can influcncc ~ h c mic:i-ocnuir-r~ritnetit foltorr.itig rlefer:ilinn anti may Jl;~vc- a

trtilizing e r c c t on scedlirlg growth (c.g. Dinerstein and 1,Vcrnmel: 198H: i Alillr) and Suirez, 1995; Ti-ilvesct ^$1d., 2001a: Cosyiis rl al.. YOOfi). I n sotnc

cil-c111n~t;lncrs. howevcr, the pccseilce of t'aeres ]night recl~lce germination sucrecs 13y hcilitatlng fut~grll arld:or I>:~ctcrial growth (Xleyer and IVitlncr, 1[)I1H). In other ritscs, farr,al tnaterial can protect sceds froin attack nf- spec-ies-specific parasites anrl precliitots (R-agnsn ?l (I!., 200:1). T h e rather sparre studies on this stlhject Il:~vc reported that the rn;~tcl-ial the tlispersed FCCCES i11.c rntbetlrled in is another lactor that 11ret-Is to he consirlcrerl w l ~ c n cvalu;~ting the iufluence o f Irugivorcs o n the final b t e r,F sccrls trf [Ieshy- liuitrrl plants.

The number and combination of seeds in the faeces

Srerl-mix~ng may alho it~nucnce gern~ir~ati.nn a ~ l d l o r \redllng g ~ o w t h , 1 ' 1 1 ~ tiumI>t-r of'srecls clefer.atc-d In a rlroppirlg can br very relevant to the futtlrc csral~li.ihmtnt succcs\ nF a plant. l701 instance, a meclia~risrn ofat~totoxir itv m i g h ~ explain the it1vcr5e ~r~rrclatic>n between seer1 abuntl;~nce i111~l g~rrttinatinn suLtrss fc)unrl by Rarnca d ( d . (1992') Ibr Snhrt~tt)a hrt~bwm anrl

A4onrs ~iigra. -I'll? I)l.csencc trf a large quantitr uu seecls in a r l i - o ~ ~ ~ > i i i g can i11sO inlli~cnce hotli post-dislw1-sal ?it.erl predation (e.g. Jnnzen. 1 !)Pli:

Sclil~pp. 1990; Traveset, ll)!)O: R.errntijo ^F!d.. I ( - I C ~ X I - a11rI intra- at>cl intcrsprrihc cotl~pt.~itir~n (e.g. LnisrlCe. 1 g00). 11) atltli~lnn. wlien different seed species :ire clcfccatccl it1 the samr r l r c ~ l ~ ~ i r ~ g , i~ ic po';sild~ t11n1 tllic or lnorc lnay ex11iI~if allrinl~atIiic cnccts t11at in~>ihit tjir g r i - l r ~ i n a ~ i u l ~ O F r 11c crther- spccics (hIayrr anrl R~ljilkoff-~iayl>cr, 1L9X2: CipalIi~li ancl Lcvcx-,

!!1!)7).

Effect of frugivares separating pulp from seeds (delnhlbition)

In drupes ancl bc1.t-irs, seeds are si~r-rouncled by a layrl- oi fl~s11 o r p l ~ l p that 0ffrr.s ;t I-ewarrl 10 fr,k~givt~tcs but may alsv have vtl~ri- runr~iorls cr~rli ^,IS the 111-utecticln o f the seeds anrl the prevention of-grrminatirm I V I I ~ I P s~ill ^{I F I ~} llie plant (Evcnari. 1949; Mayet- anrl RlljakoII-hlavber, 1982). Tlii.;

inhi\)iltinn can take several 601-nls. Tlte irlhitition may l)c intlucetl hy high osmotic prrsrul-t, sattsed by tlie high sugai- contcnl c>f I-ipe fi.i~its (Samucls alrcl 1-eve);, 2005), hy light-blocking pigmer~tatiun that pr-events ctiough light reachin5 the aerrllinps to srimuIate ge~nninatiun (;I pc>saihlc rcnsncl

t l . 1 1 ~ nlaliy ripe fruits ai-e ilarkly pigmentecl; Clpollini and Crve?-, 1!)1)7). o r fi-om sec011d3ry rnetabulites that directly ir~hihit seecl germinat in11 (Evrn;~r-i, 1!14!); Cipollini atlcl Lcvcy. 1997). Althr>tlpil irl rnosz cascs the cxarl rneclimism is not knorm, illany t a l ~ o ~ x t t ~ r y studies have confil-mrrt 11la1

~ c c d s orten fail tn gcrminare in I k r i disl~es M ~ I I P ~ ~ ill it~wct Inlit, whilr rliry

~-eadity gel-initlate wlicn hancl-cleaned. Foi- exarriplr, li0'2. of t h e 46 rvnor'lv species that are rlispcrscrl bv birds in New Zcalanrl showed poot- germin;ltinn ^(<'IOf;C) in rri~its. Ilowevel; foi- most of ~llcsc spccles.

germinatiorl of hat~cl-clcalled seeds was > !)I)?> (K(Eir11\. rl d.. 20W4). .4 recenl rrvie~r. (Rohrrrso11 rt 01.. 2OUG) sl~orved thnr more t hi111 Imlf nl- tIrc species

~cstecl foi- drinliil~itioil sl~nvcrl strons effects of it.inouing rhc pulp on sced gcrminatioil, though in tnost cascs tests were cuntlc~rtetl it1 F'etl-i rlishcs.

wliicl~ appear rn p'-o~lut:c arrilicjally large eflcctn c-r)inp;ll-ctl wit11 tests conductet! in ille firlrl ( R o c l r i ~ c ~ c z - [ r e pl d., 3105: K<~lw~-tson ef a l . . 2006;

sec discussion below). 7;) dc~rrrminc t l ~ c extent tn which the sclcasc 01- sccds !torn tlie pulp is a critical step in allo\\ping grr~rlit~ation, it is i n i p r ~ r ~ a r i ~ that ~licse rests ai-e also ci~riclucterl in lield conditions, wllrl-c r:lirinical Icacliin~ and biolc~gir.~il P L - ~ C C S S ~ I I ~ arc quite rliftel-l-nt t i o l r r tltnsc i n llle laboratory.

In ii f c ~ cases, there is dii-et11 tvidetlcc of- ~ I ~ c ~ i i i c a l inllil>itio~k ~f

~ e i - m i ~ ~ a t i o r l Irom constitzteiits in the fruil p i ~ l p . Etg~I-tasl~i p1 n l . (1!1!)H) I'n11nr1 that while seerls 01- Snrlttls cnv>nrnix/n (Kosaceae) t h;tt wert! I l a ~ ~ r l - clenncd or that llatl been inges~ed and clcfkcntrl-l by duqkv thriisht-5 ( 7 i t d t t c

rararl~ri~t?ini: Turcliilae) gerrr~i~~aierl equnll!. urcll in the latmi-atur~~ sseerls that wrr-e eirlier. within intact fruirs u r r x l r i ~ c t ~ r l aticl trca~ccl rvitln a 1% s<~li,tir,ri of pulp j ~ ~ i c c , railed to gerlninatr at :111. This si~ggcsts that ^:j sri-c>~rg cherr~ic-al wllicli it11iil)its germinatir~n oc-rt~r-F in the pulp. T h e a c r i ~ r

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82 A. Travssst et al. Role of Endozoachory in Seed Germination 83 rt~mponent(s) was (were) not iclentifed rn thih care. Kichrrlond and

Gliisalhertr (1994) fot~tld a si~nilarlj' strong inh~bltian of seed gcr~nrnaliur~

in F:~:lpn~~lf~ltlfilfl ~tlrtlcrrlntn (Myol~ornccae) k o n l extracts of the Fruil waI1 01-E.

rrmr~rl~/cr anrl E. ~-r~crmos(c. Tllr active ingredient in this case was ten~atively idcntilied as a n aromatic slycuside. 1,V;lhaj rl nl, (1998) icd artificial a g x 'Fl-uits' containing Solo?~zrm anzr~?con~mz (Solai~acrae) secrls and low concentratiuns of two na~urally occurring S. a m ~ ~ i c n n ~ t l r ~ glycualkaloi~ls to ccdar waxwings (Rol~l!~?rtlkr crrll-rw~tnz; Rornbycillidae). TIIC collectrti sred<

Tronl tliesc 'fruits' sI~owetl rrrlucrd gel-minalion rates comparcd witti seeds cullectetl ruflowing rlelecation from agar 'fruits' that conraincd no ,@ycoalkafoi~ls. This suggests t l ~ s r r thcsc glycoalkaloids can maintain bin- logical activity as g e r m i ~ ~ a t i o n inhibirors even aitel. gut passage. and t h a ~ they may have additional roles as allelopatliic s ~ ~ b s t a ~ l c e e acting on other potentially cotnpeiing seeds FolIowi~lg deposition in Faecal clumps. WC will I - c t ~ ~ r n to this idea when we cunsider rieposition patterns.

Effect of fruglvores on seed scarification

T h r seed coat is, to a varial)le extent, rnccl~itnically nndlor che~nicalJy scar~fierl when passing through the digesti~e tract o f a frugi\,ol.e. T l ~ c level nT scarification depends upon: (i) L I I ~ spccies OF frugivor-r. that ingests llie Irliit: and (ii) thc inrrinsic wails of rhe fixits and seeds, T11c fl-ugisorcs' morpl~ological and physiolugical traits, as well as retention times in rile gut, can alter the exteii~ ^tr,which the seer1 coat is rnoclified ( e . ~ ^Vuri-ayet n l . , 1994; Trareset, 1998; Tiaveset vt rrl., 2001b; Figuerola PL al,, 2 0 O P ; S;lrltamaria ^P! d., 2002; Charalan~hidrrl~ P! ( l ! . , 2003, ?005: Pollux et m!..

200.5). Impc~rtant ~norphological traits incl~irle the length or the digest1r.c tract ancl the PI-escncr of a gizzard; physiological traits inclurle digestive fiuids in t h e g11 t (w1iich can i7;117. [Irpe~ltlillg upon rhe type uf foud inges~c.cl along will1 the rruits), water content, p14 and proportion o r ptant n~atei-ial.

1.ikewise. ~,ctcntio~r time can depend upon a ~)ariety of Cacters. F~trther- more, pF:ui~ w i t s s ~ t c h as pulp cornpusition, seer! age, sccd size, ctlat thicknrss and teutul-e also influence the degree uf ~r-arificatir~n. For instance, thc pulp nray have laxative co~npounds which prornotc a faster wed rlcposition (\furray el a l . , 1994; W h a j et al., 1998) ur conslipativt.

uuhstanccs that slow it down (Cipollini anrl Levey, 1997).

A lung rct cri~ion 1.i1ne can bc clisadvantageous I~ecausc she clipestivr fluicls to rvhich seerls are exposed may damage the cmbr?,o anrl thus rlecrcasc seed viability (Jarlzcn rl 01.. T9X5; Murray ^P(nl., ^II104:Santamarin rt d., 2005: Chalalarnbirl~>u rl rrl., 2130.5; Pollux et d., 1003; hut see Meyor a n d Witnler. 1998: X2.hIiaj rt a!., Ig!lH). Hecause l a y c seeds generally have l i n r t e r rercntion times in t h r gut (1-evey ancl Grajal, 1991; Stanley and l.ill, 2UO!?a) we mighr expect tlicir germination tu be less alTected by digestive iluirls than that uf small seerls. Hort.cvcl; ail ~nterspecific curnparisr,n in a mew-analysis f u ~ ~ n c i thilt species with largc sccds shorvecl mure effrrc~s

or

ing-csrion on ~crrninatiun (rorrl1la1-ecl with hand-clcaned seed) than species

r v i t l i slnall seeds (Traveset and Vcrclli, 2002), a l t h o u ~ h this diffel-encc w a s no longcr sigiiificalll uIicri the metrl-analvsir was phvlo~cnrtic~llv contl-ulled (Verclb and fiavcset. 2005). T h e r ~ f o i e , rhe implica~lcirts of sretl size for gern~ination after passage t I ~ m ~ i g I r an animal's gut retnain unclear and are prokal~ly species-rle[)e~idcnt. hlu~eover, secd FIPP 1s not a l w a ~ s col-ielatcd with retention time in the gut, as rcccntly found in thc duck- dispel sed pondweed, Potmuo~cto~i p ~ c t i ? ~ a t ? ~ ~ (Polaniugeto~~aceae, L.

Santamaria rt al.. ~ ~ n p u l ~ l i s h e d result^). More rla~a are certa1111v needed I,r>th on thc ac~ocia~ion helween seecl s i x and gut passase time and on the efrect of S I I L ~ time un germinatio~~ performance, cspccially for f~-zlqvores ntlier than b~rds. Givcll the d~fferent lood rrtcntirm tltrlrr that occur among diKcrc~tt rrugivore taxa (Tor irtstance, between small hirtls ancl norl-flying malnlnaIs o r reptiles), we might expect stronx diKccrc11ccs in the cffrct 01- sced size a n retention time in the gilt among tliesc Iri1givo1-e gro~lps.

In a recent study that co~ripared t11c e f f r c ~ uf diffei-ent guilds or Frugivores on thc germination of Ifit620 jl~rticnscl (Rul,iitce;x), Nugales rt 01.

(200.5) found hat stierls ingested Ily squirrels (..llln?rtoxena g t ~ t l u s : Sciul.irlac) or ral)l~ils

( W C ~ O ~ I L ~ I ~ I

c ? i n i m l ~ ~ ~ ; Lepoi-idae) were less vial~lc ancl gcrrninntcrl in lower propel-tions than sccds itlgcsrcd l)! either hir(ls o r lizards. They artributcrl this rliffcrencc to ~ I l e rrliicli Iongel- retention time uf seeds in the digestive rracrs of t h e rnan~rr~als. S.eetls fulluwing 6-ugivor-c gut passage harl a much t h ~ n n c r coat than uningestcd scccls, prcsumallly d u e In differences in the late of seed-coat erosion (Fig. 4.1). I n thc hiediterrancan species

1217fll1,r co~lilr~linis (Mvrtaceae), ~crmil~rition responses also diffei-er1 acor~i-rling to the species of frl~girore (Travcsct ^F!al.. 'IOIJlb). Again, tt~ese rlifFere1lc:e.i

\\.ere artrihutcd to the longcr retention times [IT seeds iri mammals co~npnrccl with birds. 13owever. l t ~ e Fruir~ ol'otlrei- spw-ies OF plant ingestrd by c-liff'crc~lt Crugivnrcs will1 very diffcwnt rrien~icln ~inics showed no differ-enres in sced germination response m v e s e t and \t7illson. 1E197:

Nogales 1.1 d., 2005: Rodrig{irz-P6rez et nJ.. 2005).

The nreta-analysis pct-lormed by Travcsct and Vcrcli~ (2002) IurtIicr revealed t l ~ a t fri~givnr-e taxoIiomy has a n important cmect on sccd g-esm~nation respol-iscs. This analysis s h o ~ c c d that bats ^;111dbirds tcnd to gcrm~nation percentages, comparcd urth uningt.steci seet1.c) w l ~ e ~ e a s ~ r o n - rig~1ific;dnl ^cffrcl, althollgh the 11urnher ^of exp;ri~neii~s with ^thrse Fruyvores is st~ll small (Traveset ancl Verdil, 2002). Fishes could not be

~ n c l ~ ~ d e d in the nnalyscs due to the sca~city or c1;rta on this grorlp clcsplte thetr iniportancc as scccl dispctscl.~ in Inany riverine systems. Such rliITcier~t effects among rruglvore tarra arc again attrihutcd, at lcast ~)artlv, to thr rl~ffrrent foorl relen~ion ritnrg, whicll i~ gen~rally longer in non- flying rnarnnials and reptilcs than in birds and bats. Birds that include large amounts of f r u l t ~ In t l l ~ i r dicl llavc a proportionally shorter intcstinc ancl a smallrr and less ~llrtrr~rlat g i 7 ~ a r r I than non-F~ugivn~r,us hirrEs, whicl~

may result in a mure ~ e n t l e treatment of thr Loat5 of srcrlh iiigmtc-d 11%

speciali\t fi I ~ ~ I V ~ W S (1'1illlainen rl ul., 198 1 ; Jordatln, 2000). Morpllologic;~l

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84 A. Tfaveset et al.

U U cmtml r +&XI C-S AN8nlox~nrs

5

- ₂

^l00

Lanzamte

2

90 L I

S ,

80 ' /

I

Fig. 4.1. Change in seed coat thickness found in Rubra fnrtimsa seeds after being ingested by different seed d~spersers. l~zards (Gallotia atlantfca), warblers (Sylvra spp.), ravens (Corvus corax), squ~rrels (Atlantoxerus getulus), gulls (Larus cachrnnans) or rabbrts (Drycto1agu.s cuntculus) in (a) Fuerteventura and (h) Lantarote (Canar~an Arch~pelago).

Cross-sect~ons of a seed d~rectly gathered from a fnr~t (a) and of a seed defecated by the squ~rrel (b) are shown. More deia~ls of the study can be found In Nogalas et al. (2005).

rnc~rliiicntinns arc alsq hitttd in h-ugivoroir~ I-eptilcs anrl l~ats; ~ ~ r l l i k e I~ircls, in thc\e arli~nals, frrigivorrs gcnerallp l i m e I(rngcr intcstincs tl~ari inscctirtlrr,us s1)ecle.i (Kiwi a n d Il~galls, 199,1; King. 199fi).

Cninparative rests uT the \cariiicatian cflect pi-oducecl by rlifierent frltgivores feeding. on the same plant species oftcn reveal I a q e clifferences ^- s t m e imparting a gcmiirlation enlianccmei~t, c~thers iirl inh~bitrrr-y effect, and nrhcrs a n r ~ i t r a l erect (scc review in Tlavesct. 19118). Likewise, rhc same spccics o f Crugivo7-c may h a w cliilerent eKccts or1 gcrm~nation rlrpencling nprw the specirr of plant sttlrlied (Traveuet. 1993; -11-aveset rl rrl., 200 1c: Kotlrig~iez-P4l.e~ ^{p t}ol., 2005). To further cxaiiiinr these patlcrns, we coinpilecl two databases: one wit11 a tntal uf 9 studies in which percentage secrl gcrrninaeion o l a given spcclrs of plant was con~parer! bctwren ^alleast two dispel-ct.rr, and anothcr ^{( i t} = 40 stclrlirs) it1 wliiclr the ell'rrt or a rli\lwrsc~ was cornpal-er{, in the sanic snirl?., wirli at least ^{t w u}different s ~ ~ ~ ~ ~ ' . i r s o f p\allt. For rarh database, a consistc~lcy illclex (del,el~rlcnt var-ii~ljlc) rcas tlrCi~~t.rl as the fi-~quency

or

the mosr conurlon effrcl (pu%i(ivc,

Role of Endozoochorj in Seed Germination 85

~legativc ot- l l ~ ~ l t ~ - i l l ) rlivided by the total rl~~rnhel. n!" sl~ccics ~ e s l r d (eithrt- r1iq)ersci- or- p l a ~ ~ r , respectivelv). -1-hc inrlepeilrlci~t fartc>~-s wmcrc the apcric5 of rlispersc~. ^{i t 2}tltc lit-st dat;tl,nsr, a ~ i r l ~11c specie\ t)lpIat~r in the second. T11c cfict of different rlisprl-~ers 011 tlie sarne plant was fount1 tn he I I I ~ I - c consis~cilt t h a ~ l the efTec-t uf- a singlc disl>ri-wr owl- difft!rcnt pl;u~ts.

Consistent ^cttkctso n gr~-~~iirt:~tion (pu.iiti~c, t t c ~ ~ l i v c o r neutial) ^5%-el-e observed in 68.8% uf the cascs cump~r-i11g tljc ellkr:t o f tlilCcrenr ~ I ~ Y P C ~ . S P T <

o n thr satnt. plant, 3 r d no significant dilkl-et~ccs in t l i p cnnsistenc? index rvfien c o m p ~ r i n g fiugivuse RI-tyktps; X" 3.23, = :1. P = 0 . 3 5 7 ) . l n cui~trast, C C ) I I S ~ S ~ C I I C ~ was rnltcli lunmcr (33.8%) rrrhen a hitlglc dispel-sri- was testet1 with cliffcrei~t plants (X' = ??.H, c![ = I , P < 0.000 l ) . mTl~esc I-e~ults i111ply that t l ~ r pnrt~cular- scccl cliar:~ctcristicc r)C each plan1 (c,& scctl s i x . pulp cni~rposition, seed coat tI~icknesa. lextl~re) Ijromote tr~~rt-e consistent i ~ e ~ p o n s r s than rhc spccitic rnorpt~olugic:al ar~tl!c>r phvsiu1ngic-al waits of Frlrgivores,

Despite llie hct that scccl tl-am, rat11e1- tllan IFugivort. traits, drminate tIlc eflccts uf gut passagc on gesminaticm rcspunsr, i i u g i ~ n i - r s also contribute to the l~etcrogeiiei~y of-gerrnir~ation responses but11 within plitl~t popl~laric>ns and ~vithir~ plant cornrnuniries. This Iletcro~eneit!: wirh car:ll hpccres uf fr.rlgivur-e havlrlg a particulai- tlCcct on ~ l l e weds of each plarir conslumrd, migl~t he espec~ally rr~caninghrl in ltnpi-rrlictai~lc c l i i ~ ~ ~ t c s , such a5 those ti~urirl in areas ~ ' i t h unpi-etlictahlc t a i n l ~ ~ l l patlrr-ns. Fur irlstance.

t1itfe1-rnt studies in the e:tstc.rn ancl westcrn Merliterranrall basin (i711aki and Safiiel, I Y!)O; Barlle;~ <l a l . , I g ! ) l ; 'liavrset ^P!01.. 21301 11,c) hrixr tijt~ncl that the seecls of a p;irti~lildr sprcies t>f plant a r e dirlkrentially atlbctt.rl I)!, pass;ige t11rougt1 rhc guts ot" dilIP1-ent bircl species. Ileterogcncity rd' arcri rcspullsrs occurs also at a n iiltraspecific Icve[. Meyel. and IVitmrr (1 !IIlS) 1,cportrrl indiviclual dilkl-eiic-es rr.ithi11 Put rlirs ;~ii-gtu~nrin IRt)sace;ie) in gcrolini~tion respnnwcs. att~-il~utlllg tlierr~ to diflrr-r~lccs in fi-uit t~uti-irrlt c<)mpositic)r~ as xvt.II as in the irinorrnt of Fsuit plrlp arcl~nlpanying the srrtl.

A reren ^ts ~ i ~ c l y 1,crfotnlecl wit11 I'hilljrpn r n z p r . r t i / n l i ( ~ (Olcac~at.) ;1nd :I,fytt~\

~ - o t r ~ r r l z ~ l ~ i r ruitlr the grlal of i r l r l l ~ i f y i n ~ mecllanislnn that call rsl)lnin rllc dimerenl gcrminat ion responses itsually r)\)scr~e<l, shou'cd tli;~l m ~ ~ c h illlet-- and intraspccihc r.aria~ion exists 111 cliffrre~l~ srcrl-coat traits. Such lraits arc: pe~-~ncnbility coat tliickncss, texlurc (nieaslz~~ecl h)- c o r n p u t i ~ ~ g an index frr~ni a digitill itnage uhtaincd in thc scani~iirg clectrol~ rnicrosrc>pc) a ~ t d seecl hardness (ot)~nir~ed tly illcans <>F a tcstiry ~rlachine (c-on~pressinti motlc) that measures the load neerlcd to hrrak oprn lie scetl (11. -1i.avrsrt.

J . Rotlrigtiez-PCrcz and R. Pias, unp~tblishetl results); var-iatian i r l ill1 these ti-aits has beer1 found ^LO he sssociarcd wit11 variation in gel-~r~itration rcsponscs. This ilrlplics ~Ilat, wllcn cal-rying out ~ t u d i c s ^{t r y}tesl thc rRect7 of cnrluzoorlir~l-?- on reeci germination, it is ilrlpni-tan( rn incl~lde in t h r rrqts seer!< Crom ^;I ~rprcsent:lti~fc samplc uf' i!~rlivirlunl pl;tnts. Less variatloti in getinination Ins hreu found ; u u o ~ ~ g rntli\-idualr within a spcc~cs n f FI-ugivore (A. Travrset.

1.

Rr,rlri~11e7-ft.r~cz 11nd U . I'ias, unp~lblisl1erl rectilts), a f t l ~ c ~ t ~ g h i t I - e ~ r ~ a i n s irn1lr)l,tarlt ^tr, lcst ge!-n~ilialion rl~illg as mally inilirirltla) a~liin~tls xs possible.

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86 A. Travesetet al.

Effect of manurelguano an germination and seedling growth: comparison among frugivores

T'he Taecal lnareridl a ~ m m p a t i y i n g ver tel)r:1te-rlicperret1 seeds at deposition sites can play an ilnpurtant rofc in enhancing seed germination and reedllng survival (e.g. Dincrste~n ancl 'h+'cmlncr, 1985: Traveset PI d..

2001;i). .41thougl1 the iertillz~ng eff'ect or such material has been

;~cknowlrrlgr:rd dtrlorlg ecologist< ct>ncerrletl ruibI1 sred rlisprrsal h?' vrrrchratcs (lt7illrrm anti Travewt, 21300), frw data exist that test the s i x of this cffcct. Most i r ~ ~ g i v o r c s havc a very varied clict, whicI1 results in a highly variable manure composition: t h s is especiallv ctrirlent in ' c d r n i \ o r o ~ ~ s ~ tn:llntnals t11at scasurlaIly consume gtedt qr~antrties oF fruits (see, e.g. Heriera, 1989: Willson, 1993). T h e h e t of bears, for instance.

consists of vertebrates and invertcbrarcs, as r%,ell as plant material such as Iri~its, stcms, lcavcs 01 roots (Traveser rl cl., 2001a). Bear nlanurc consrsting of animal ~naterial showed a consistcntl) grcatcr cffcct on sttcdlli~g growth of Ihcc~ntnm spp. (Er~caceae) and K u h .~i)~cloh~ltr (Kosaccacl than bear manure consjsting of vegeta~io11 fib-e or fleuhy pulp (Fig 4.2; l i a ~ e s e t r! n1, 200Ia). While protein in the diet promutes a supply OK nitrogen In thc facccs, bones pl.ov~rlc a soiucc of calcittm

Fig. 4.2. Mean (e SE) seedling length of (a) Vaccinrurn ovaltfolium/alaskaense and (b) Rubus speclabilis seedlmgs In different manure treatments. Poztlng so11 was used as the control.

Flgures drawn from data extracted from Traveset et al. (2001 a)

Role of Endotoochory in Seed Germination 87

phospliatc, wllich map limit g r o w ~ l ~ in pnni- soils ^srrrhas those in the tcmper-are I-ainfurest of- AIaska (ZVillstm r t al.. 1998). C>ther components of the rnantlre nlay supply some othcr nrltricnts or inrprove the moisture rcgilne Ihr seetllings. thus explaining the greater secrlling g r o ~ ~ t h ^{i l l}du11g corn p a i d witEl thc co~ltrol (potting soil). Such restllts arc mr~sistent xith thaw rcl~orted in othcr ^sturlirs. Dinerstein a n d \Vrrnmer ( 1 9x8) Gl11nd ^;E significant increase in seedling RI-owth o i 'liaw~rr r~ird~porn (Eup hurbiaccac) wllcn secds wrtc ernhedcled in ~I~inoc-ri-ou dung cnniparrd with those grnrcing on potting soil. Sinlilarl!; srredliug g r t w ~ l ~ of several Arnrio (hfimosaceac) species in dung varied signifranr ly lletrvre~~ h e sl~ccies or cons~~rning Ilerhivoi-e, probably o w i n i to diffel-ewes ill the nritrleut contcnt anrl ill the bvatei--holcling capaciry oi'tfie clung (hiiller, 1995).

As ~rrcll ar promoting seedling growth throirgli a fe1-tilizer effect, fi-u$vore manure may also contain tuxic cornpou~lrl~ rl~ar can havc ncgntive rffects on seccl andlor seedling survival (i!cIcl~, 1!JX5; 3laralnbc ^F!ol., 1993;

Malo and Sndrcz, 1995: Cosyns ^P!d., 200.5). Animal wastes arc known to contain phenolic cc)~llpounds and fatly acids that act as gei~nination inhibitors Tclr sume plants. These cotnpo~rnds may alter the acti~rity ol- en;.ylncs that regulate ~ l l r late o f germination (Maranhe et al., 1993, and references tl-icrein). klui-euvel: fruit pulp can also provide a substrnu~ fur the gro~.tll o r fungi o r bacteria. which can be very detrimcnra1 Tor gel-minatiun or for s ~ e d l i n g survival (Mcyct. anrl I,Vitmel; I99H): thus, despitr consuirii~~g l a ~ p e cl~iantities of- fruits, cedar w a x w i n ~ s wcre Crl~~~>rl t o he incffccti~~c rlisperscrs 01- plants such as I.i?~rlfin h ~ n s n l n (lauraceae) and Pnr?llss i~ir~itli(~:rrltrr (Rrj\;~ceae) becausc a1 facc;~l aur-un~ulation al.ounrl certls. In contrast. 1.ohi11s rliil lint 11avc tllese ~legativc effects on thc germinaticln ot rl~csc spccics as they ilsualIy regurgitate the serds clean (Mcycr atatl U'it~nei; 1998).

T h e tliKet-ellcc in t l i r infIuence or rnanure from l i t ~ g i v o r c ~ I,elongir~g to (lifferrnr vrrtehl-ate tasononlic groups on seeclling cstal)listr~~~rr~r surces7 is likely to be great. T h e nutrlhei- a n d density ol- cccrls in Faeces, wlrich is knou.n to aikct sccrl nrlrl ~ c r d t i n g survival, is much I~ighrl- in Irugirorous mammals tha11 in most t)irrls (excepting casst~i~~aries, emus ar~il colonial

~ ~ c s t i n g Ilirc-Is: A.J. I>ent~i\. Qrreensland. 2005. ~>el-rclni~l uummunication I or- reptiles (Uarnca rt (d., 1902; ifTillson, 1993; h r l r e s e n and L e v y . 200-1, anrl rcfwenres !herein). T h e large nurnlwr nFseeds in the dung ol~aninials like rhinoccr-os, elephants o r hears can ntt racr <red predators, mainly i,clden~s ( l a t i z c ~ ~ . 1986; Traveset. 1990; \\'iIlsnri, 1 993; Rerlnqjo rl d., 11198;

;lntIi-esen and Levc): 2001), a11d afirl- grl-~nination, sccdliligc 21-c likely ro encounter intense cornpetifion (I.ewis, 1987; Loiscllc, 1990). Otl tlre o ~ l i r t - IianrF, the rich arirl copiuus ell-rjppie~gs of a large n ~ a l ~ ~ t n a l pro~,icle morc

~luh-iclz~s t o a scetiling, over a longcr ~)criocl o f tilnc, than the small scats of most ljirrls ^191-li7ards. IR addition, I~irrls ex(-rere I-elati\rely high anlnunls o f white mates when eating i~~vertel>r-atrs, but w;ltery matrrial olten colo~.lr-rd wit11 h i t pigments when c n ~ i n g Triiitu. \\!ll~le it seertls clc;lr 11r;lr ~ I i r variation in lijccal cornpc>sition bctrr,ccn disl~cw;~l ;Igmrs migli~ a i l c c ~ scctl and scedlirrg pel-fc>i-mance, little is ct11.1-e11tlv ki1o~r.n. Thur; it \r.oulrl IIY 1rseTu1 to illvcstigate this in future s t ~ ~ d i e s .

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88 A. TFaveset et al.

The effect of seed aggregation$ and seed mixing on germination (allelopathic and density-dependent effects)

Drpcnc1iti~ cm a fr~lsivore's ~ i z e arrcl heflavinul: scccls tllat have bee11

~,cgtitgitatrd 01- cleft-(.atecl r\.ill hc clepositrrl over a ~vidc I-ange c>f dcrlsities ancl with a varying dcgrec of sprcics-mixinx (Stilec a n d IVliitc, 1!M:

Jr,rdano, 2000; Fig. 4.S). Regurgiraroi-S tcnrl to prncrsc iruirs ancl rlr-<)p rl3cnl cme a1 a tirrle t~rncatll the marernal wcr, with little specirs mixing; and (lie d i - ~ ~ p l ~ r t l seeds may acc~unulatc to high rlc~lsirirs (Stilcs anrl

\Vl~itc, Ic3SF; Stile?;. 'lnO0). In contrast. fruit-ingestit15 fr.rrgivt)res tlcposit scrrls in Caec;11 rlrimps aftcl- gut procrs5ing. 7-lie degree rll- clustei-ir~g of thrsc setrls clrpcl~ds OII tlie size rX the laecal c l u n ~ p alltl the rlcnsily of seed\

in e;~cli r l u ~ n p , as well as on whcrlier tlirrc is all aggregation oi clllllips I>cnr;rrlr 1-r)t)sting ^01-nesting tree>, latrines br orher regt~!n~-ly used locatio~ls IL)rbussclir p t (I/.. 198"; D e l ~ ~ ~ s s c l i e nnrl Isen~nann, 1994: Deal1 ant2 Miltnil.

2000: Stiles, 2000: Takahastri ant1 Iialnitani, 1003). The degree o i seed- niixiilg and the cl~nrrce of- rleposition rui~h I~~tcrospecifir neigltllouru nlsc!

\,a1 y wirli thy size uf the frugivorr anrl ~ h c gilt-retcntior~ tirnt. (Stiles anrl

\Vliite. l!)HG: Jorcla~ln, 2000). I.arsr a~iiriials rrilrl t n clepo~it clrrmps with nioi-e scedc and more seerl-tnixirrg th;it> du s~nall h,u~ivores.

h-~lgjvoi-cms t~ircls ~ypically rlepnsit ~ w o o r more species it1 d~-(lppitigs.

1.oisrlle (l9!)0) rrcnrtlcrl an ~ v e l - a g e of 132 srccls rxf 2.3 plant sper-ies per rl~,ol~ping in five spccics of's~rlall rrx rnerlitum-sizecl frugivnl-ous pxserirlcs i l l

(:rrsla Kic;a. Stnnle): anrl Lill ( 2 0 0 2 ~ ) ib1111d that in a tcnlpente wonrllancl ill A~istralia, tl)c wl~itc-e?-e (ZO,\&~Y>~,< Irrluml~~; Zosbrropidac) deposited on aver;lg

"-2'15 s e r r l ~ of I .l-1.3 species pet- rlroppit~g, and the sllpelG Bir-y- wren (;21d/in!,5 ,;\.(I~PII; 5ialtrr-itlac) abour 4-10 seerls of just one sprc:ics. I n rrlnti-acr, one Cassr~waly rlrnpping {l:rr.r.nnrirrs rn+~,nn?r\; C;rsr~ariirlac) in North

Fig. 4.3. Faecal clumps varj greatly tn slze from (a) b ~ r d dropptngs (from a New Zealand prgeon) w~th few seeds and a small amount of guano wrth one or two plant specles. to (b) Large m~xed species communal dung prles of large vertebrates like these white rh~no latr~nes In South Afr~ca wth seedlings of the rh~no-d~spersed Datura $p The env~ronmental opportunrtres and challenges are obvrously very d~fferent In thelr two extremes and are lrkely to have jnfluenced the evolut~on of fruit and seed tra~ts

Role of Endozoocho!y in Seed Germination 89

Queenslanrl was found to contain l S 'mui-e nt. l r s s intact 6-clits' nf Ruil.vclmrrrrlic~

sp, (Laul-aceat), each wrth a d i a i ~ ~ c l e r ol allnut G cni :itid rveighinp itruur~rl 52 g (Stocker and Irvinc. 1983). ^?']I? Asian rhinu (Klli7lo(-vm~ I~ ~ / K o I ? ~ D : Kllinoctriaticlac) dispel-ses seeds in huge dcleti~tions that can weigh u p T O

23 kg and prrsmmably 1)otcntially contitiri ~housands of seeris (Dinrrstein ancl 1,iJenirner. 1988). Arnazanian r\'oolly monkey rlroppi~lgs we\-r h>und t o cont.i~i~~

an avciaKe or 70 seeds ol 2.33 spec-ies (Ste~wnson. (;haptei- 15, this vrilumel.

Pine atid stulle nlai'ten (13klrlr~ 313flr10 and i7.I. foina, r?spcftivt.l?-, Irlus~pliclac) scats r~ollcctc(1 from a r\.oorll:r~lrl in Gel-rn;iny c:tlrltainrtl on avrragc nhout PO0 sccds per scat nf a variety of fleshy-fi~~itecl species [Sclta~tnlann and I-lci~l ^ken.

2002). 171us, dcpcnding 011 rhe irtrh.ivore, rlepositecl seeds nlal- find rhr~nselvrs at IOW bcnsiries in t l ~ c L~eccs trr. as part nf a I:rr~e assemblage OF cunspccific or hetti-ospecitic scetls competing [or space, light ancl n1111-icnts.

'I-Iiese very cliffrre~~t envirrrnmrnls pusc clillcrcnf ecolo$al oppr>ttiunities and challenges, anrl if- tliel-e is a consistcllt pattcr'n tn ~ h c depclWtion conditions, there Inay l ~ e seleclinn p]-essures fui the evnlution of npprupriate gerlninarion stl-ategies (Idi~lI~art, 1976: 1.uisclle. E I190; Mrli-1;1?: I<)YX). I11 ninst cases, der~sit~-de~e;lrlen~t bctors will tend ¹⁰impact ttegatively on the success of seedlings ;is they coniprtc for rcsnurces and sl~al-c (I.e\vi~. 1987; Lniselle, IIIRO), so ~elcctinn will tend to l)e Tor tactics tlial give an arlv;uua~e tr]

seedling in this competition. Pcltrntinlly these tar~ics rnay ~ndritlc early gcrmin;~tion to !,ear the rush, or incll~red clonna~rcy 1 0 wait niit the r,mwrl (I.oisellr, 1990; Mitrr;~y, 1998). ~lllrcrnat ivcly, s r e t l ~ rnav prod~tce allelrqlathrc uhemiciilu

-

nr use tltore contained in fruit pulp

-

tliat are aclivc aaitinrt cror~specific or heteraspt.cifrc neiglibnul-ing sccds.

Therc is an extensive literature r r i l t h e involvcmerlt of altrlochr-mirals finlncl in the seeds aticl fruits nf- dry-kuiteci sllecies, pal-tir.~llarfy in agriculture. Piall~s that I~zvc been sliorvn to pr-urlt~ce w;rtcr-snlul>lc set-nii- nation inhibitors that arc poteut against olllcr pasti1l.c plants in~lurlc tllr tliistles C(II$IEPIS n~rlnns ant1 (Inofloiullr~rr arrr~tllrirrrr; (Artcracrat.: IVardlc r f n l . , 1991; Qadri-i pt ral., 2003), Hishop's vicecl A w w i I I I ~ I ~ I F (Xpiarene; Frict-binan a/ d., 1982), I ' i p n 71~vr~tgo (Fabaceae; Surni~n ^tt^{U / . .}200'21 and Lolrri t w ~ v t i ~ (hbareae; 1,aterra ancl Dazzalo, 19001.

Apart h-on1 the eviclcnce of p r ~ l p inhibi~ors mrntiunetl carlicr (whir:li have all been tester1 o n cnnspecilic.u), we are awi11-e of only one sluclv uf a fleshy-fi-uited spccies tliat has demonstrated active allclochrmicals tllnt are effcctire (in he~erospecific seetl.;. HI-tiska cl (/l. ( I Y R I " ) used a CUL-11rnhr1-- srerl bioaasay to irlentifv gcrlnination irillibitors froin tllc lily i . i l j f l p ~ I ~ I I T C L ~ ~ ~

(T,onvaIhriaceae), althol~gh thry did not test the rfler-r of there inliillitors un sccds of specirs h a t are likely to he consur~red h7 thc same F~-~rgivnl.cs that dispersr I.. T I ~ I I S I , ( ~ ~ ~ , ant1 the authors t l ~ c ~ ~ i s c l v r s intrl-pret the dafa =I%

evideilcc c ~ f auto-inllihitiur~ to prevent prrrnaturr aerminatinn in-Iruit rather than as evidence ot'aflelopathy. Further test< of fi-tiit consfittlents as sources or allel~~cliemicals eflectivr i r g a i ~ ~ s t potcnrial compt-litors that 31-r likely tu co-occllr within drnppings w c ~ t k l be welcome.

I n s o n ~ c q i t ~ ~ a ~ i r ~ n h , ~ l l c r e rnay he atlvanrages to :lggres;l~ecl rirl>c>sitiun patccr-11s. I < P I I ~ er o / . (ill press) clepnsilcd sreds of-il N c ~ c ZralanrI ~nistlet(x=,

(9)

90 A. Tmvesetet al.

Prrnsd1(1 t~trrr/~r/nla (Luranthaceae), on to liost l>ranches as s~nfile seeds anri

111 cluimF>b ol five. Ger~niniiticln and e\tahlishment success per suer1 was sigr~ibcantly h r g i i c ~ in the cl~imps than in single seeds. Thrs appearer1 to hr rl~re to ;in increased tendency to arihere 10 the halt branch in clulnpa.

Hr~ufevcr, over the s ~ ~ h s e q u e n t 57 month?, ~ h c r e ^ru;l~a tendrncy for sli~litly lowei rater oi survival in clumps. negating the inittaI aduanragc.

Tllc consequences of the aggregatron alseerls into cl~trnps as the result n i the feeding and dcposirion parterns of Irupr.ores ^remainsone of ^{E ~ I C} leas^ ~ ~ n d r i sroocl and \tt~diccl asprcts of seer1 dispel-s.d. Cllaracterlzillg the effectiveness OF diIIcrent fi-ugivorrc 11). theil- seed disprrsal kernclc o r b r their al~illtv to depos~t seed3 ¹¹¹safe sites ignores the potentially important citcc~s lhat nlay ocrur at tlie wale of the l~~rlivlrlual rlropping Difrerrntial nllelopath~c and competitive interqpccific effects hct~veeil seecls \vithln theso clumps made by differel~t frugivnrcs have ttlc poter~~ial to iinpose nu acldit~onal layer of complexitv that rnay distol t the view rstablisherl from simple movement pat Lerrls and grtt passage times. Mnwcx er, until we h;~x,e fttrther sturlics that test the magnitude uf these effects. ~t is cl~fl~cult to assess their likely i~nportanre for the fate 01 seed.

How

do we Experimentally Investigate

the

Factors that

Influence

Seed

Fate?

Se\.rral kcy qtiestinns have etnergerl Srorn the previous section concernillg the interactions Z)etween fi-tigivores arlrl Irurrs x t ~ d the wav that thcsc pmc:rs<es influence the success of seed gcrmina~inn. Thrst. questions are 130th etolrhgical ;incl evr>I~it~onary. have itnplirntions : ~ t tilc con~~nulrity level as r\.cll as FIN tile clemt>graphy uf individual spccirs anrl, w e believe. sho~tlrl b r or equal inrerest to tl~corcticiil and applied rcologists as well as to rvr)lt~tiona~-y I~iologists. C)Tccntritt i~riportnnrr are the fac.tc>rs that inI311c11ce the eventual Fatcs of scrrls, \ ~ I ~ i c h c311 cssentixlI!, bc boiled d0rr.n to these:

[i) s~1cccssCu1 grrminaricln and establishment to the seeclling stagy; (ii) clcath l,! pre- rlr pnst-clispci-sal

reda at ion

o r disease; and (iii) thc i n r l ~ ~ c t i o ~ l

dorn~ancy and incorporation into the soil seer! bank anpailing future oppoi-t~initics. T h e likclihoorl o l each nF lhcse i s cletcrmincrl, at leas1 it1 part, by fie inherent biological properties or the pla~lts' strategies shaprcl uvcr millennia b y natul-ill sclectiurl and alsr, lly the changing hiotic and alliutic. e t ~ v i r o ~ l m e ~ > t allcl tlispel~ral services provider1 ¹¹⁷fiugi~orcs.

1. M'hat happens to R~sIry Irriits iF thcy are riot ingestcci

-

a t e they doomerl tu [ill firor11 rlje plant attd be prrventcd lioin gerinir~atson by aiitotouic inhibitors, (11- asc they rapal>lc ot' germinating a n d maintaining tIie local popi~latic>n?

2. Does it Inattcr rr.liat type of fi-~rgivores Cecd on the rriuts? Ilo rru~iuorcs that rcgurgitatr seeris ~ ~ t . o c l ~ ~ c e rlifyerel~t c-Ii:t~lgcs in seed traits 1-elcvnnt tu

gel-rni~~atinn than fi-c~givnres thar tleiccate heeds?

3. Hurv i m p o r t a ~ ~ t is the compositiori ol-the droppings it1 which seeds are

Role of Endoaoochory in Seed Germination 91

rleporitcd? Is there i~~trrfet-enct: hctrvrcn seecls in mixed-q~ecies droppings, ant1 ^tc>what extent d o the othei- constituents of the dropping farilitntc or retal-d scerl p i - ~ n i n a t i o n ? \.Cc have come srmic rray i l l

cleter~nining [lie consequences or the tliffeferelit depnritinll Iiattenls t11at are p ~ o d u c c d by dift'erent Fi-~~girwres. For cxnlnl)lc, seecls in clense clun~ph are fi-rt111enrly worsc olf than thosr deposi~erl in slnall groul~s, clcpending mn the species. I'ti riow nced to answer questiunq suclt ^ac: (i) are early germination and allelopathy effrctivc strategies Fni- c t ~ m p r t i ~ ~ g ~milh neiglibn~r~-ing seeds; (ii) 11o1v impor-tant is tlie frr-tiliralion cfFcct and rtoes it alter the relative effrctiveness nldilfcrcl~t dispcrsers?

M u c h prngresq has been made already anrl \<*c hnvc ;it least partial answers to sorrie of these questions. Howeve!; we hrlieve tllat itirther progress ancl clarification of inconsiste~it or uncertain results wilI conw h-on1 cai-eft11 aktenrion to the design of experinierith, as rt.cll as Irom attention to same factors that hi[Ilrrto have largely been ignul-crl. ^t\ii iinportant poitlt lhat has emerged from rhe work don^ to ~ l a t ~ is the context in which experiments arc perfoi-mccl. :Is we slum 1)clorr..

cr~nducting expcsimcnts in t h r held 1-atl~cr than in the laboratory is cl-ucial Tor answering ~ h e s e questiolls i l w e ivisI1 to obtain answer5 that arc relevant tu t h r systems w e st~~cly. I11 the fullowing sections rcc autlinr seven reco~nmcntiatiorls for thc dcsign nf filfurr rxperi~nclltal st~irlies that seek to answer these qiicstir>ns.

f. Conduct these studies in fleld condltlons

T h e ~niria-ecological conclitions prevaili11g aL thc sitc ~vliei-e a srerl is clep~sirerf ^call reprcscnt another sourcc

or

i.ariation icr ^{i t s} futui-r ger~~lirlation behaviotrr. Llrls~ rcportccl infol-mation cnrnr* Cr-o~n S~LICIICI:

C:II-rierl out 1111rlel- corm-ollrtl r:ii-c-riinstanccs, usually in tllr lahr,i-:~tr~~-\ (scc I-evicw of the scarilicatiun efiect in ?i;~vest.t nilrl \ki-dil, ?002), y r t !he results n~ighr nut reflect what rertllv F ~ a p p e n ~ ill 1l;Irurc.

Or

the 83 stuc[ics co~lsidrrecl in that review. 56% testrtl srcd gel-rnination in lrthnl-atw-y conditirlns, another 22% pperk~rmed gerniinatioll cxpei-inients in he helrl.

and 13% u s ~ t l glasshouses. Only ^ilii~tall rr:~ctio~l (7%) used 1no1-e t l ~ ~ n i rlne condition. T h e ~nrta-atlalysis revealecl that lallnratnrv ntlrl ticlrl cuntliriclns wei-c rnore likclv than glasshol~se espcriments to rlctrct rlifi'crcncrrs l>ctwceil treatments (ingested vcl-sus noir-ingested seccls), althol~gh LIE^

Iorvei- sample sizc for gIasshr>usr cases rnight well have causecl s11ch clifTcrences. 11 more rcccnt an;ilysiu uf 11ie scarilication and tleir~llil~ition effects, which considered rmly bird-dispersal systems anrE ir>clurlcd some aclclitic~nal srridier that \yere not in rhe T~ravesct ancl IJcrdfi (2002) rla~nsct, suggested that, in pcncral. the dci~iliihition effect is l;tr~;ci- thi~ri LIIC scarihcation elyect, anrl that hot11 cStects a]-L' ~ t ~ o n g l v iiifl~ici~c~cl h? 1 1 1 ~

testing environment (Roherrson rl d., 2006: FIK ~4.4). Irr this anall-sis.

Faboratury stul-lies tended ^{t c j} i~irlicatc stron,qei- eflGctr liar^ citllcr

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R2 A, Ravesetet al. ^RoJe^ofEndozoochory in Seed Germination 93

- 4

Field Glasshouse Laboratory

F 0 c 4 4 -

P

"l

"?

0, m O -

-4 -

Flg. 4.4. Box plots of the relatrve slte of (a) scar~ficatron and (b) deinh~bitron effects of fruit

processing and the effects of the testing environment in fleshy fruited species. In (a) we calculated the srre of the scarif~cat~on effect by calculating the natural jog (Ln) of the adds ratios (OR) comparing the f~nal germination percentage of seeds from fruits passed through a gul versus those from hand-cleaned fru~ts in 56 specles, foltow~ng Traveset and Verdu (2002). In (b) we compared the effect of handdeanad versus Intact frults as a measure of the deinh~b~tion effect m 51 specles.

- B

plassliourc nr field 11-ials, pnrticufarlv fur- dcinf~il>itinn. T l l i ~ rriigl~t h r rlt~c In the p e a t e r pl~ysicu-chernicn1 and hir)togical processing of rrrtits anrl cce~ls tl~a! occur ^illrhe iiclrl after ~ h c y have beer] rlrpusirctl. This pnct- rlispcrsal pr-r>c-rssing inay rrplicatc or 1eplat.c t11c processes that happcn in tlir animal gut tn somc e s t m t and lie~icr ~ - r t l t ~ c c the depcnclencr 011 gut t~-aii5j>ol~l for S ~ ~ C < - ~ S S ~ L I ~ gel-~l~irlali(ln ( h l o r p e ~ h ^F! (I!., 1997; Raskin ;~nrl 13nskin. l!)!)H: hlnrpeth ant1 Mall. 2000; Knl)crtsc~~i rf ( I ! . , YOOtii.

F~eld Glasshouse Laboratory

Stuclie5 that have trutecl the scai-ilicatioii elfett ill 11iol.c than one exprt-irnental conrli~ion h a ~ e clfte~r revealer1 rather incr>i~si~lent tecr~lts (Rusra~nnntc cl n l . , 1992; De Fig~~citcrlo ar~rl Prl-in, 1993: nr Figueil-rrlr~

ancl 1,ongntti. 19!IT: Yagilia.~hi (I!.. 199s; Ti-ave~ct P/ nl., 2OOlc; Iiytrrrrja and Castr-r). 200" R~orlrigi1cz-Ptrc7 rl ( I ! . , 20115: K(7hertsnn c/ rrl . 2OOii).

XltIrou~h thc constant crl;lditions in the Iaboratoi-F ~r~iglit srem i t l r ~ l !CH- rlelecting difFP1-ences in germination t>rr\\.een inges~etl 2nd no~i-ingw~crl scctls, this va15es clepenrking upon r11r plant tested (Xlblc 4.2). Some studies Ilave rc,uncl a g1-eatcr scax-ifiratitln citect 011 gcrn~inaticlr~ i11 l l ~ c 1:ll)oratory rt>rnp.~i,cd with field c x p e r i m r ~ ~ t s (Thl>le 4.2a: ?,g. Ilust;l~n;~ntc- ^P!

d., 11192, 1595; De Figueii-rtlo and Perin, 19!45; t'agiha~hi r! n l . , I99P), while uhiets have drtrctctl an c k t or ~erminatinrl only i n o i ~ t d o o r cnnclitinns a n d nut in ;L gro~vtli charnt~el- or gIa5shr>11sc ( e . g . Travrset PI d., 2BOlc). A frw studies liilvi, f o u ~ ~ c l similar results hetween 1alicjratr)r.y a n d ficlrl concliticms (Rust ancl Rnth. 1981: RI-a1111 ancl Rraoks, 1987; Izhaki ancl Safrirl, 1990; Rarnca F / a l . , 1!)91). I n a recent stuclv, a tot:~F nl- eight species cif plants rcei-c- tcstctl bnth in an cxl~erimcnt;~l g n r d c ~ ~ : ~ n t l in [tic I~cld, ~ i l r l rinly half shc~wecl cn~isiste~lt i~csults (Ilclrlrigi~cz-l'iw rl r r l . , '.'tlO?).

Owl-all, I:~boi,atol-?~ srutlics tend ~o slmw mure helwilt ol scili-ification or1

gerermina~ion compai-er1 \r-it11 zlas<ho~lsc or held ^tests.~chicli ^cl11,lvcl,agc 4h0w t l l i ~ t scarifi~a~i(>ri makes li!~lc difrercrlrr to final get-nrir~atio~i percentage. 'l'here arr w r y Sew cases where the rlritrl~ibirion rFec-t has l~ccll meas~wcd in more tIlair orw el-ivironn~ent (lhhlc -!.?h\, t r ~ r t again rhcse t e w rliitn slrggest that the rcsrilbs rlcpel~cl very mtrcli on tht. testinz- c ~ i ~ i r o n t n e x ~ t usecl.

T h e 11~1-1iculnr cl~ai-ac:~c~,istics o f tlie habitat rllleie thc ger~ninatic~n tcsts arc pei-lilt-tr~ctl in the ficrlrl Inay also a k c t the I - ~ ~ L I ~ I S . Fat. itistance. ^{1 1 1 ~} sallnitv or the soil wllctre seeds wcrc sown rzmas iniind t r ) ii~iluc~rce gcrnlinar ion responses 111 two spccics or haluphytes (l.:spiiial- r/ ^01.-',00-i).

-ll~crctbre, if rlur ~ o a l is to cval~iirtr rr81iethel- a ul~angc in gel-~rlinatior~

oulromcs i s atbptive or c l r > l , ir is c r u r i ~ l I hat scccl I-es1it)nses to rlisprl-ce1.s'

#tit treatment ^;Irecxarnincd in the ticld, in conditions t l t a ~ arc h i r ~ ~ i i ; ~ ~ , ¹⁰ tlir)sc. rnrtwr~terctl h! the subject pl;lnt. T l ~ r lahoi-aton rs u+rltil i n r rxalnining tie u n d e r l ~ i ~ l g mcchanisrnu rmce a li~lrl cspei-init.111 Ilns cletern~ioer~ rEiat the nutconles ai-e in~portant. Espinar rl 01,'s (2004) findings

;~lst, highlight the nett1 to corlsitler tht. hctcvogrrrc.it?. 01- tlie Eiahitat ~n the experin~ental design, as tliis rnay he all additirrnal ~ u u v c c of v;~riation in several sturiies on post-dispersal seed prerlation. gel-inination sllrce+ a t ~ d seedling est;lhlisllrnent ^(?,g.I-lcrrera PI n l . , IC194: Srhrrpp. 19175: Rcy ;111tl

Theory and its Application in a Changing World