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
Contents
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0 CAB Intei-rlalio~~al 20[17. 2 2 1 1 1-ights rescrvrtl. No pal-t orthis pu1)lication may be
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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. UK
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 on Different Conrincnts 5
! : - J f . fi)~g~l, A, [ D ~ T L I $ , X J 1\fazf7. I'A. . J OJ I WI ! , 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 mk
3 The Evolutian of Visual Fruit Signals: Concepts and Constraints 5')
H.IIJI. S r h o ~ ( ~ l . onrl I! SC~( I P{ YT
4 A Review on the Role of Endozoochory in Seed Germination i H
A. 7jr~1zl~srt, A. 11' Rohu~tson orid.]. Rr ~Er i f l r r - P~TPY
5 Living in the Land of 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, PR. CZI ZJ I I I I I ~ET 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 ~
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~ge fraction dl i vi ng plnt~ts pmrlucr fi-llits that attract a~limals (W7c anrl
27% ol- gyrrlllosperm and 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 (IVilIuon and 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~~gi vorcs 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 pl ~~s i ol og~e s (IT the digtstive tract that af kt l the
survival probability of rlw ingcstecl secrls in diflercnt ways (Hrrrci a 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 rdert r~ct . s thereill). T~liercfore, the specilic seecl
~r ai t s irl an 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 t h~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 esami ni t ~g the elycct of a sced's passage through a
rri ~~i vni -e' s gut, i ~nd give Lilrthrr rlircctiuns on metfiocls for l ut ~t r c stutlirs.
FI-nil treatimcnt in thc disperser's tli~estive tract (which includes pulp
separatior~ from scerls and trentmrnt of the seeds) can determine the
capacity of sccds trr gel-mjnare and, thus, is one of 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 ~t i l re nl ' t l ~r relationship.; I~el ~vccn
fruit chr r ~ni st r ~ and moi-pt~ology ancl tIir typc of- clisperser. i s crucial to
unders~aildillg thr co-evolutivn of- pl ant -r~-~~gi rore intrl-actinns ( C. $
Murl-ay c! 01. . 1994; Cipnilini and I.evY!,, 1995; \2::1h;?i P! d., 1991;: Ke pn rt
d., 200 1: 'I'P~cksbnry and Nabl ~an, 200 l ; \IJcnny, 200 1 : S~anl cy and I-ill.
20Cl2b: Al dnt ara allcl Re?, 2I103).
Biology of the System: From Fruit SwaElowing to Seed Fate
Frugivorcs that slvallow fruits (subsequrntly rcicri-ecl t u as rr~~gi vares) 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 al ~l i s hc~l [Table
4.1). f3elo1v we briefly nutline the i s~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 by secondary 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 wi t h~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.)
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 nhj l ~t i cl ~~ (tlie rlrit~hihlrior~ e Rc 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 t hr 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 andl or chemlcal scarification of the seed coat or endocarp
T h t rffcct ol'scarificat ion 1s u\i~all? t l ~ougl ~t to rlcprnd on rctet~tion t ilnc in
tllc drgeqtivc t~.lct ancl on the type of rood i~rgcsted along wlrh \reds
(Rarnea p t a / , 1990; %avcset. 1995). T h ~ s mechanisln (ratller tIiatl
ctrirlllib!t~c>n) i s t hy 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 ect eni~~il.ical
cvidrt>ce of wch a l t c ~~~r i o n of t l ~c scerl coat or. endoca~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 er cct on scedlirlg growth (c.g. Dinerstein and 1,Vcrnmel: 198H: i
Alillr) and Suirez, 1995; Ti-ilvesct $1 d., 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 (Xl eyer 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). The 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 wl ~cn
cvalu;~ting the iufluence o f Irugivorcs on 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 i t ~nucnce gern~ir~ati.nn a~l dl or \redllng g~owt 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\ nFa plant. l701 instance, a meclia~risrn ofat~totoxir itv
mi gh~ explain the it1vcr5e ~r~rrclatic>n between seer1 abuntl;~nce i111~l
g~rrttinatinn suLtrss fc)unrl by Rarnca d (d. (1992') Ibr Snhrt ~t t )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~XI - a11rI intra- at>cl
intcrsprrihc cot l ~pt . ~i t i r~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 gr i - l r ~i na~i ul ~ OF r 11c
crther- spccics (hIayrr anrl R~ljilkoff-~iayl>cr, 1L9X2: CipalIi~li ancl Lcvcx-,
!!1!)7).
Effect of frugivares separat i ng pulp from seeds (delnhlbition)
In drupes ancl bc1.t-irs, seeds are si~r-rouncled by a layrl- oi fl~s11 or p l ~l p
that 0f f r r . s ;t I-ewarrl 10 fr,k~givt~tcs but may alsv have vt l ~ri - runr~iorls cr~rli ,IS
the 111-utecticln o f the seeds anrl the prevention of-grrminatirm I VI 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). or
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 al ~o~xt t ~r y studies have confil-mrrt 11la1
~ccds 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 he 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 ~l l csc 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 ( Ro c l r i ~c ~c z - [ r e pl d., 3105: K<~lw~-tson ef al . . 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~rl i t ~at i on, it is
i ni pr ~r ~a r i ~ that ~l i cse rests ai-e also ci~riclucterl in lield conditions, wllrl-c
r:lirinical Icacl i i n~ 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 i s dii-et11 tvidetlcc of- ~I ~c ~i i i c a l inllil>itio~k ~f
~ei - mi ~~at i or l Irom constitzteiits in the fruil pi ~l p. Etg~I-tasl~i p1 nl . (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 i nges~ed and clcfkcntrl-l by duqkv thriisht-5 ( 7i t dt t c
rararl~ri~t?ini: Turcliilae) gerrr~i ~~ai erl equnll!. urcll in the l at mi -at ur~~ sseerls that
wrr-e eirlier. within intact fruirs ur r xl r i ~ct ~r l aticl trca~ccl rvitln a 1% s<~li,tir,ri
of pulp j ~ ~ i c c , railed to gerlninatr at :111. Thi s si~ggcsts that :j sri-c>~rg
cherr~ic-al wllicli it11iil)its germinatir~n oc-rt~r-F in the pulp. The a c r i ~ r
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) konl 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 ~sr r thcsc glycoalkaloids can maintain bin-
logical activity as ger mi ~~at i on inhibirors even aitel. gut passage. and t h a ~
they may have additional roles as allelopatliic s~~bst a~l cee 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
Th r seed coat is, to a varial)le extent, rnccl~itnically nndlor che~nicalJy
scar~fierl when passing through the di gest i ~e tract of a frugi\,ol.e. Tl ~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 ext ei i ~ tr, which the seer1 coat is rnoclified ( e . ~ Vuri-ay et nl . ,
1994; Trareset, 1998; Tiaveset vt rrl., 2001b; Figuerola PL al,, 20OP;
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 he 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 or ptant n~atei-ial.
1.ikewise. ~, ct cnt i o~r time can depend upon a ~)ariety of Cacters. F~trther-
more, pF:ui~ wi t s s~t ch 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 al . , 1994; Whaj 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 r r l . , 2130.5; Pollux et d., 1003; hut see Meyor
and Witnler. 1998: X2.hIiaj rt a!., Ig!lH). Hecause l a y c seeds generally have
l i nr t er rercntion times in t hr 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) t han species
r vi t l i slnall seeds (Traveset and Vcrclli, 2002), a l t hou~h this diffel-encc was
no longcr sigiiificalll uIicri the metrl-analvsir was phvl o~cnrt i c~l l v
contl-ulled (Verclb and fiavcset. 2005). Ther ~f oi e, rhe implica~lcirts of sretl
size for gern~ination after passage t I ~m~i gI r an animal's gut retnain unclear
and are prokal~ly species-rle[)e~idcnt. hlu~eover, secd FIPP 1s not al wa~s
col-ielatcd with retention time in the gut, as rcccntly found in thc duck-
dispel sed pondweed, Pot muo~ct o~i p ~ c t i ? ~ a t ? ~ ~ (Polaniugeto~~aceae, L.
Santamaria rt al.. ~~npul ~l i s hed result^). More rla~a are certa1111v needed I,r>th
on thc ac~oci a~i on helween seecl s i x and gut passase time and on the efrect
of S I I L ~ time un germi nat i o~~ 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 or reptiles), we might expect stronx diKccrc11ccs in the cffrct 01-
sced size an retention time in the gilt among tliesc Iri1givo1-e gro~lps.
In a recent study that co~ripared t11c ef 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 gt ~t l us : Sciul.irlac)
or ral)l~ils ( WC~O~I L~I ~I c ? i n i ml ~ ~ ~ ; Lepoi-idae) were less vial~lc ancl gcrrninntcrl
in lower propel-tions than sccds itlgcsrcd l)! either hir(ls or lizards. They
artributcrl this rliffcrencc to ~Il e rrliicli Iongel- retention time uf seeds i n the
digestive rracrs of t h e rnan~rr~als. S.eetls fulluwing 6-ugivor-c gut passage harl
a much t h~nncr coat than uningestcd scccls, prcsumallly due In differences
in the late of seed-coat erosion (Fig. 4.1). I n thc hiediterrancan species
1217fll1,r co~lilr~linis (Mvrtaceae), ~crmi l ~ri t i on 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 ~i ni cs showed no
differ-enres in sced germination response mv 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 ~at fri~givnr-e taxoIiomy has an important cmect on sccd
g-esm~nation respol-iscs. This analysis sho~ccd that bats ;111d birds tcnd to
gcrm~nation percentages, comparcd urth uningt.steci seet1.c) wl ~e ~e a s ~r on-
rig~1ific;dnl cffrcl, althollgh the 11urnher of exp;ri~neii~s with t hrse
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~ral l y longer in non-
flying rnarnnials and reptilcs than in birds and bats. Birds that include
large amounts of f r ul t ~ In t l l ~i r dicl llavc a proportionally shorter intcstinc
ancl a smallrr and less ~llrtrr~rlat gi 7~ar 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
84 A. Tfaveset et al.
U U cmtml r +&XI C-S AN8nlox~nrs
5
- l00
2 Lanzamte
I
2 90 L
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 f nr~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 ~at s; ~~r l l i ke I~ircls,
in thc\e arli~nals, frrigivorrs gcnerallp l i me I(rngcr intcstincs tl~ari
inscctirtlrr,us s1)ecle.i (Kiwi and 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 aqe clifferences -
st me imparting a gcmiirlation enlianccmei~t, c~thers iirl inh~bitrrr-y effect,
and nrhcrs a nr ~i t r al erect (scc review in Tlavesct. 19118). Likewise, rhc
same spccics of Crugivo7-c may ha 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 al least
two dispel-ct.rr, and anothcr ( i t = 40 stclrlirs) it1 wliiclr the ell'rrt or a
rli\lwrsc~ was cornpal-er{, i n the sanic snirl?., wirli at least t wu different
s ~ ~ ~ ~ ~ ' . i r s of 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
cfi ct 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 cttkcts on gr~-~~i i rt : ~t i on (pu.iiti~c, t t c ~ ~ l i v c or neutial) 5%-el-e
observed in 68.8% uf the cascs cump~r-i11g tljc ellkr:t of tlilCcrenr ~I ~YPC~. SPT<
on t hr satnt. plant, 3 r d no significant dilkl-et~ccs in t l i p cnnsistenc? index
rvfien comp~r i ng fiugivuse RI-tyktps; X " 3.23, = :1. P = 0. 357) . 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. l ext l ~re) Ijromote tr~~rt-e consistent
i ~e~pons 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, drmi nat e
tIlc eflccts uf gut passagc on gesminaticm rcspunsr, i i ugi ~ni - r s also
contribute to the l~etcrogeiiei~y of-gerrnir~ation responses but11 within plitl~t
popl~laric>ns and ~vi t hi r~ 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, mi gl ~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 ai nl ~~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 al . , I g! ) l ; ' liavrset P! 01.. 2130111,c) hrixr tijt~ncl
that the seecls of a p;irti~lildr sprcies t>f plant ar e dirlkrentially atlbctt.rl I)!,
pass;ige t11rougt1 rhc guts ot" dilIP1-ent bircl species. Ileterogcncity r d' arcri
rcspullsrs occurs also at an 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 t s ~i ~cl y 1,crfotnlecl wit11 I'hilljrpn r nz pr . r t i / nl i ( ~ (Olcac~at. ) ;1nd :I,fytt~\
~-otr~rrlz~l~ir ruitlr the grlal of i r l r l l ~i f yi 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 cl i ffrre~l ~ srcrl-coat traits. Such lraits
arc: pe~-~ncnbility coat tliickncss, texlurc (nieaslz~~ecl h)- cor nput i ~~g an
index frr~ni a digitill itnage uhtaincd in thc scani~iirg clectrol~ rnicrosrc>pc)
a ~ t d seecl hardness (ot )~ni r~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 ~Il at , wllcn cal-rying out ~t udi cs t r y tesl thc rRect7 of
cnrluzoorlir~l-?- on reeci germination, it i s ilrlpni-tan( rn incl~lde in t hr rrqts
seer!< Crom ;I ~rprcsent : l t i ~fc samplc uf' i!~rlivirlunl pl;tnts. Less variatloti in
getinination Ins hreu found ; uuo~~g rntli\-idualr within a spcc~cs nf
FI-ugivore (A. Travrset. 1. Rr,rlri~11e7-ft.r~cz 11nd U. I'ias, unp~lblisl1erl
rectilts), af t l ~c~t ~gh i t I - e~r ~ai ns irn1lr)l,tarlt tr, lcst ge!-n~ilialion rl~illg as mally
inilirirltla) a~l i i n~t l s xs possible.
86 A. Travesetet al.
Effect of manurelguano an germination and seedling growth: comparison
among frugivores
T'he Taecal lnareridl a~mmpat i yi ng 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 ~~gi vor cs havc a very varied clict, whicI1 results in a
highly variable manure composition: t hs is especiallv ctrirlent i n
' c dr ni \ or o~~s ~ tn:llntnals t11at scasurlaIly consume gtedt qr~antrties oF fruits
(see, e.g. Heriera, 1989: Willson, 1993). The 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~nt nm spp. (Er~caceae) and K u h . ~i ) ~cl oh~l t r
(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 srrrh as 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. t hus 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 ~ort ed in othcr st urlirs. Dinerstein and \Vrrnmer ( 1 9x8) Gl11nd ;E
significant increase in seedling RI-owth o i 'liaw~rr r~i rd~porn (Eup hurbiaccac)
wllcn secds wrt c 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 l l et rvre~~ h e sl~ccies or
cons~~rni ng Ilerhivoi-e, probably o wi 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~l rl ~ 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 of germination (Maranhe et al., 1993, and
references tl-icrein). klui-euvel: fruit pulp can also provide a substrnu~ fur the
gro~. t l l or fungi or bacteria. which can be very detrimcnra1 Tor gel-minatiun
or for s~edl i ng survival (Mcyct. anrl I,Vitmel; I99H): thus, despitr consuirii~~g
l a ~pe cl~iantities of- fruits, cedar waxwi n~s wcre Crl~~~>rl t o he incffccti~~c
rlisperscrs 01- plants such as I.i?~rlfin h~ns nl 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).
The tliKet-ellcc in t l i r infIuence or rnanure from l i t ~gi vor c~ I,elongir~g
to (lifferrnr vrrtehl-ate tasononlic groups on seeclling cst al )l i st r~~~rr~r surces7
is likely to be great. The nutrlhei- a n d density ol- cccrls in Faeces, wlrich is
knou.n to aikct sccrl nrlrl ~cr dt i ng survival, is much I~ighrl- in Irugirorous
mammals tha11 in most t)irrls (excepting casst~i~~aries, emus ar~i l colonial
~~c s t i ng Ilirc-Is: A.J. I>ent~i\. Qrreensland. 2005. ~>el-rclni~l uummunication I or-
reptiles (Uarnca rt (d., 1902; ifTillson, 1993; hr l r es en and Levy. 200-1, anrl
rcfwenres !herein). The large nurnlwr nFseeds in the dung ol~aninials like
rhinoccr-os, elephants or hears can ntt racr <red predators, mainly i,clden~s
( l at i zc~~. 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 ari rl 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 of tilnc, than the small scats of
most ljirrls 191- li7ards. IR addition, I~irrls ex(-rere I-elati\rely high anlnunls of
white mates when eating i~~vertel>r-atrs, but w;ltery matrrial olten colo~.lr-rd
wit11 h i t pigments when cn~i ng Triiitu. \\!ll~le it seertls clc;lr 11r;lr ~ I i r
variation in lijccal cornpc>sition bctrr,ccn disl~cw;~l ;Igmrs migli~ ai l cc~ 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 ~~di es .
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 and 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 t o 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 cl un~p alltl the rlcnsily of seed\
in e;~cli r l u~np, 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 pt (I/ . . 198"; Del ~~~sscl 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 or more species it1 d~-(lppitigs.
1.oisrlle (l9!)0) rrcnrtlcrl an ~vel - age 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 ( 2002~) ib1111d that i n a tcnlpente wonrllancl ill
A~istralia, tl)c wl~itc-e?-e (ZO,\&~Y>~,< Irrluml~~; Zosbrropidac) deposited on aver;lg
"-2'15 s er 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 $p The env~ronmental
opportunrtres and challenges are obvrously very d~fferent In thelr two extremes and are lrkely
to have jnfluenced the evolut~on of fruit and seed tra~ts
Role of Endozoocho!y in Seed Germination 89
Queenslanrl was found to contain l S 'mui-e nt. l r ss intact 6-clits' nf Ruil.vclmrrrrlic~
sp, (Laul-aceat), each wrth a di ai ~~cl er ol allnut G cni :itid rveighinp itruur~rl
52 g (Stocker and Irvinc. 1983). ?']I? Asian rhinu (Klli7lo(-vm~ I ~~/ KoI ?~D:
Kllinoctriaticlac) dispel-ses seeds i n huge dcleti~tions that can weigh up TO
23 kg and prrsmmably 1)otcntially contitiri ~housands of seeris (Dinrrstein ancl
1,iJenirner. 1988). Arnazanian r\'oolly monkey rlroppi~lgs we\-r h>und t o cont . i ~i ~~
an avciaKe or 70 seeds ol 2.33 spec-ies (Ste~wnson. (;haptei- 15, this vrilumel.
Pine atid stulle nlai'ten (13klrlr~ 313flr10 and i7.I. foina, r?spcftivt.l?-, Irlus~pliclac)
scats r~ollcctc(1 from a r\.oorll:r~lrl in Gel-rn;iny c:tlrltainrtl on avrragc nhout PO0
sccds per scat nf a variety of fleshy-fi~~itecl species [Sclta~tnlann and I-lci~l ken.
2002). 171us, dcpcnding 011 rhe irtrh.ivore, rlepositecl seeds nlal- find
rhr~nselvrs at IOW bcnsiries in t l ~ c L~eccs trr. as part nf a I:rr~e assemblage OF
cunspccific or hetti-ospecitic scetls competing [or space, light ancl n1111-icnts.
'I-Iiese very cliffrre~~t envirrrnmrnls pusc clillcrcnf ecolo$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~si t ~-de~e; l rl en~t bctors will tend 10 impact 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 t r ]
seedling in this competition. Pcltrntinlly these tar~ics rnay ~ndritlc early
gcrmin;~tion to !,ear the rush, or incll~red clonna~rcy 10 wait niit the r,mwrl
(I.oisellr, 1990; Mitrr;~y, 1998). ~lllrcrnat ivcly, sretl ~ 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 he 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 i n~l url c tllr
tliistles C(II$IEPIS n~rlnns ant1 (Inofloiullr~rr arrr~tllrirrrr; (Artcracrat.: IVardlc r f nl . ,
1991; Qadri-i pt ral., 2003), Hishop's vicecl Awwi I I I ~ I ~ I F (Xpiarene; Frict-binan
a/ d., 1982), I ' i p n 71~vr~tgo (Fabaceae; Surni~n t t U / . . 200'21 and Lolrri t w~vt i ~
(hbareae; 1,aterra ancl Dazzalo, 19001.
Apart h-on1 the eviclcnce of pr ~l p i nhi bi ~ors mrntiunetl carlicr (whir:li
have all been tester1 on 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 YRI " ) 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), al t hol ~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.. TI ~I I SI , ( ~~~, ant1 the authors t l ~c~~i s cl vr s intrl-pret the dafa =I%
evideilcc c ~ f auto-inllihitiur~ t o 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 gai ~~st potcnrial compt-litors that 31-r
likely tu co-occllr within drnppings wc ~ t k l be welcome.
I n s on~c qi t ~~a ~i r ~nh, ~l l cr 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 Nc ~c ZralanrI ~nistlet(x=,
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 hr gi i c~ in the cl ~i mps 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 ~~hs equent 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
ni the feeding and dcposirion parterns of Irupr.ores remains one 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 or br
their al~illtv to depos~t seed3 111 safe sites ignores the potentially important
ci t cc~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 pot er~~i al 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 i s cl~fl~cult to
assess their likely i ~nport anre 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 xt ~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 FI N tile clemt>graphy uf individual spccirs anrl, we believe. sho~tlrl
br 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 or disease; and (iii) thc i nr l ~~ct i o~l
dorn~ancy and incorporation into the soil seer! bank anpailing future
oppoi-t~initics. The 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 by natul-ill sclectiurl and alsr, l l y the changing hiotic and
alliutic. et ~vi r o~l me~>t allcl tlispel~ral services provider1 117 fi ugi ~orcs.
1. M'hat happens to R~sIry Irriits iF thcy are riot ingestcci - at e they doomerl
tu [ i l l firor11 rlje plant attd be prrventcd lioin gerinir~atson by aiitotouic
inhibitors, (11- asc they rapal>lc ot' germinating and 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 . oc 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 mpor t a~~t is the compositiori ol -t he 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 do the othei- constituents of t he dropping
farilitntc or retal-d scerl pi - ~ni nat i on? \.Cc have come srmic rray i l l
cleter~nining [lie consequences or the tliffeferelit depnritinll Iiattenls t11at are
p~oduccd 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 ~ mp r t i ~ ~ g ~milh
neiglibn~r~-ing seeds; (ii) 11o1vimpor-tant is tlie frr-tiliralion cfFcct and rtoes i t
alter the relative effrctiveness nl di l fcrcl ~t dispcrsers?
Much 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 hr held 1-atl~cr than in the laboratory i s cl-ucial
Tor answering ~hese questiolls i l we ivisI1 to obtain answer5 that arc relevant
tu t hr systems we 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
The ~niria-ecological conclitions prevaili11g aL thc sitc ~vliei-e a srerl is
clep~sirerf call reprcscnt another sourcc or i.ariation i cr i t s futui-r
ger~~lirlation behaviotrr. Llrls~ rcportccl infol-mation cnrnr* Cr-o~n S ~ L I CI I CI :
C:II-rierl out 1111rlel- corm-ollrtl r:ii-c-riinstanccs, usually in tllr lahr,i-:~tr~~-\ (scc
I-evicw of t he scarilicatiun efiect in ?i;~vest.t nilrl \ki-dil, ?002), yr t !he
results n~ighr nut reflect what rertllv F~a ppe 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 il ii~tall rr:~ctio~l (7%) used 1no1-e t l ~ ~ n i rlne
condition. The ~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 i i i fl ~i ci ~c~cl h? 111~
testing environment (Roherrson rl d., 2006: FIK ~4. 4). I r r this anall-sis.
Faboratury stul-lies tended t c j i~irlicatc stron,qei- eflGctr liar^ citllcr
R2 A, Ravesetet al.
RoJe of Endozoochory 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. Tl l i ~ rriigl~t h r rl t ~c
In the peat er pl~ysicu-chernicn1 and hir)togical processing of rrrtits anrl
cce~ls t l ~a! occur ill rhe 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 t n somc es t mt and l i e~i cr ~- r t l t ~cc the depcnclencr 011 gut
t~-aii5j>ol~l for S ~ ~ C < - ~ S S ~ L I ~ gel-~l~irlali(ln ( hl or pe~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 nl . , 1992; De Fi g~~ci t crl o 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 . 2OOi i ).
XltIrou~h thc constant crl;lditions in the Iaboratoi-F ~r~i gl i t srem i t l r ~l !CH-
rlelecting difFP1-ences in germination t>rr\\.een inges~etl 2nd no~i -i ngw~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 xpe r i mr ~~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! nl . , I99P),
while uhiets have drtrctctl an c k t or ~ermi nat i nrl only i n oi ~t door
cnnclitinns and nut in ;L gro~vtli charnt~el- or gIa5shr>11sc ( e. g. Travrset PI d.,
2BOlc). A frw studies liilvi, f ou~~cl similar results hetween 1alicjratr)r.y and
ficlrl concliticms (Rust ancl Rnth. 1981: RI-a1111 ancl Rraoks, 1987; Izhaki
ancl Safrirl, 1990; Rarnca F/ al . , 1!)91). I n a recent stuclv, a tot:~F nl- eight
species cif plants rcei-c- tcstctl bnth i n an cxl ~eri mcnt ; ~l g n r d c ~ ~ : ~nt l in [tic
I~cl d, ~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 t est s. ~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 wr y Sew cases where the rlritrl~ibirion rFec-t has
l ~ccl l meas~wcd i n more tIlair orw el-ivironn~ent (lhhlc -!.?h\, t r ~ r t again
rhcse t ew rliitn slrggest that the rcsrilbs rlcpel~cl very mtrcli on t ht . testinz-
c~i ~i r ont nex~t usecl.
The 11~1-1iculnr cl~ai-ac:~c~,istics of tlie habitat rllleie thc ger~ninatic~n tcsts
arc pei-lilt-tr~ctl in the ficrlrl Inay al so 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).
-l l ~crct bre, i f 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 cr ur i ~l I hat scccl I-es1it)nses to rlisprl-ce1.s'
#tit treatment ;Ire cxarnincd in the ticld, in conditions t l t a~ arc hi r ~~i i ; ~~, 10
tlir)sc. rnrtwr~terctl h! the subject pl;lnt. T l ~ r lahoi-aton rs u+rltil i nr
rxalnining tie unde r l ~i ~l g mcchanisrnu rmce a l i ~l rl 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?. 0 1 - tlie Eiahitat ~n the
experin~ental design, as tliis rnay he all additirrnal ~uuvcc of v;~riation in
several sturiies on post-dispersal seed prerlation. gel-inination sllrce+ a t ~ d
seedling est;lhlisllrnent (?,g. I-lcrrera PI nl . , IC194: Srhrrpp. 19175: Rcy ;111tl
94 A. Traveset et al. Role of Endozoochory in Seed Germination 95
Xlcintara. 1200C): Ti aveset et al . , 2U05: SrZiupp, Chapter 20, this vrllrtmc).
Placing sccds into the field rcquires a technique drat allorvs the fare of
seed tu he rasily foiluu.ed. Kobertsou rt al . (' LOO(j ) I I S P ~ small scctiuns of
pipc partly pushed into the liltet. layer and laid o ~ t in a regular ai-ray tu
i~ll+>\\' ~ a s y clrecking of gcrn~ination ant! ~.ccovery OF seeds by s i e ~ , i ~ ~ g
the tube contents at the enrl or cxperimrnt 10 cljeck [or viability. Ot l ~et .
options for I-efucating l ayer seeds i ~l cl t ~de tiny n~eral tags clr monofilamcnt
wire tethers atlacheti t n thc I~al-d pal-[% or scrtls (ser, c,:. hIuClritincss,
1997; SterIe P/ (d., 2001 : 1.i and Zl ~nng. 2005). Fol-gc~ and !2'cnnc (2003)
provide ;I ~ e v i c ~ v of technirlrtrs used to iblloiv seer1 b t c , some of which ins!-
Ix npplicahlr 1.ogernrin~~ticrn stllclies.
2. Recognize and appreci at e t he distinction between t he speed of
germination and the final germination percentage and avoid talking
about t he rate of germination
Gerr~~illittion pei-fbrmance may l ~ e ineasr~i-er1 I~ot h hy the p~-oylr)~-~ir,il ol-
seecls that have get.mit~ated ;Ir the ctid of- the st~rrly arrrl h!, the speed wi t h
wllicli sceds germinate. Cunfilsingly both have t)Ttc.il Ixen ter~ncrl
ger ~ni nat ~nr ~ 'rates' and this should be avnirFcd 111 tutu1.c studies (Rnbel.tson
cl c l / . , 2006). While he hr r ncr is positively i~elatccl to fitiwss, the ~ccond is
nor nccehsaril\, as [or i ns~i ~ri cr, early grr~ninateri serrls might be rnrJl,e
IikcIy to dic nF desiccation, pa~liogens, predators, etc. (I~-~\ rcsct . 1?98, ancl
1-r~rrcnres therein). Seeds that ilo r w l ger-minntc immertiatrly. or that rntel-
dt>rlnnncy may nevertliclcss cunti-ihutt. significnritly t<) pl;lnt Ltncss h?
riicpersi~~g in time I-ather than In space anrl may rrniaill in waiting for
suiri~l>le conditions ( K~l l y * t al.. 2004; Rrh)t.rtaon et d.. ?00(i). 11 i s 11icrcC01-r
r~nrrl~rvhile desci-ihina 't>oth thc distr-ibutiun or ~i nl i i i , ~ of grrlilinatirln as
we11 a.; I-ecr,i,cling the f nal pci,cclltagc or scerl ~cr mi nar i un ar ul r.llcrking
ful- <l(lrit~ant sceds in tlie retrlainclcn
3. Measure the deinhibition effect as well as t he scarifieatlon effect
Several recent papers I l i ~ ~ e nutccl the cunf~rsir)i~ in the litci,ii~ure about the
poccSses that cjccilr duri ng g u ~ passagc, ancl have empl~asizrd tllr twcd trr
Ineasiu.r Imth r>utc:on~cs of gut paswgc: t I ~c cleinliibition cilcct as wrll as the
scariiicatio~l effect (Iklly et 01.. 9003: Samucls ancl I.rvey, 200.5; Rohei -~so~l v1
d., 200ti). I f we a ~ - e l r ! answer the fil-sr l\vo questinns (1 ;tincl 2) irclui r l ~c
p~evi ous s~cti on, we 11ecd rn cnrtlpare the perforrtlance ofsecrts from thi ee
ty'prs n i rrcatmrnt: (i ) manually extt.acrccl from the pzrip: (ii) iruact l i - ~~i r s:
n11d (iii) sredr that have been ingested and regurgitarcrl nr rlckcarecl 11r
Gugivurrs. IInmparing (i) anrl (iiil is a test of tile scatiticarir~~l erect , rr.liilr
comparison of (i) ancl ( i i ) i s ;I tev of thc deinhihitir>~l eltcct. Conrpaj-ing ( t i )
;u~rl (iii) alluws ilrl assessment cif the ct)mbinril efrrr:t or I)ntlr processr5. 111
Sa n~~wl s :11111 LCVC~' S (2r10.5) I.~-V~CII' 0f-!111 SIII[I~CS. 77% uf- rllrst. rr~nsiclel-er1
96 A, Traveset et al. Role of Endozaochow in Seed Germination 97
unly the scarIhcarir>ll elTrcr. Ilcjnc !neasui-rd siniply tlrc rleinl-lihiric>t~ cftccr.
atid cm!!, IHrJ illclurlrtl all thl-PC ti-ea~~iients ant1 c o ~ ~ l d tllcrrfoi~c cstii11;lrc
tlie ilnportaiice nl I~otll etlrcts. .l'he r en~ai ni ~l g 4% c o ~r ~~~a r e c l seeds fi-urn
i n~nct li-!tit$ and thnse tlrfecatcd ~ J V 6-uKivort.s and so wtl1.c nrlt able 10
scparatr rlcinhit~ition allcl seal-ification rfkcts. Th e surve) OS thc rclntive
efTt.r:t sizr I)y Kol ~et t so~l P! ( / l . (2006) mgge.;ls that the rleinhikirion eKcct is
clltel~ largei- ~Ii an the scarific,ltio~i rfltct, a l t l ~ t l ~ r ~ l ~ since mt.vst sturlies werc
ct,nrl~~ctetl in Pc~I-i .~Iishes which tlo not appear to acc~u;\tel!, preclirl t hr
clfec-~h in tlir: iicld, fin-111cr 1.1~111parisr)nx arc n~r t l ccl fl-ntrl field c-ot~dit.io~is.
4. Allow sufficient time for seeds to germinate, and recover ungerminated
seeds at t he end of the st udy to check for viabilityldormancy
As inclicaterl above, sccrls ha w tlit-ee fates Following dispersa1 - death,
gcrrni~l;~tion 01- seconrlary clorniancy. Dis~inguishing between dornlant and
tlcatl weds is important, sincr tlie lbrnicr may allr>w seeds to enter thc soil
secri tlank (Iiell? r/ # l . , ?004) and cn they s~~nul cl 1101 be as~ul ncd to he clcad
(13nskin i~ncl Raskin, 19!)X; Kohett.son cl ( I ! . , 2006). Some seccls 11);1y 'take
several years to germinare. For ecample, scecls of the Ncw Zealat~d
gyrnt~nspr~-tri hit~~nrr~~il~.~jrnrrgi~~rn (I'c>rlocarpareac) werc still gel - ~ni ~~at i i i g
in fielrl conditions inure than 4 years after birtl irigestlon (Clout and ~ille!:,
1992). Sceds that ai-r I-ecnvri-err nray lle tcsterl for viirl~ility eir11c.r with
tetl-;i~oliiim rl~loricle (Cattiell. 1947) or pl:tccd i11 idcal laboratory
ct~ncliriolln I'ol- ~c1-1nini1tio11.
5. Consider the influence of other components in the diet of frugivores
'The rkict of $1 pnrticirlar species of disperse- is kunwrr to alter. i i x~!
rcte~rrirln time. For instance. E~uupc a n starlirlgs ( S ~ ~ ~ I ~ I Y I . \ ~~i i g~- ( ~l or l r i r :
St ~l i . ni rl ~e) shoscretl rter-rei~sed g111 11)3555:1ge t i i i i e~ ~b'lien rlrcir rlie~ was
ch;~nged G-o~n irlsccrs tr, tiuits ( I i i t ~~s ov anrl Lcvry, 11190). I . i kcwi ~e, a scecl-
I);~sccl, Iiigh-hbre diet has hern fi)ril>c! 10 incsmsc seecl digestibilit! i l l
~nnllarris ( ~I t i or j~lt1/~~-11?nrl1~1,1'; :\~~;llirlae) ancl ge1-minatir>ri o l seeds nf
I'r>ln~rlr~gr/n~z prt.tn?n!lrs decl-eased as seed I-etcntiun lime I r i the clucks' ~ u t s
iucr~a.;erl (Cliaralalnhirlt)~~ pt ( I / . , 2005). 1:rw w;~tt.rlowl, grit quantity
(sri-niiyly relatctl to diet) it1 t t ~ r gizzard <:an also l ~avc largt. cirects t)n seed
gcrniirrability ( e. g. 5ant;lmasia tf nl . , 2002). Tliur, for lirtu1-c i n ~r c r i ~t i o i i s
cm rile cfterr? nI- seer1 ingestion by di spcr s~ss on gel-minatior~, it i s
importalit to rrbaitirain ;~ninrals 011 the same diet whet1 performing
exy)trimcills in cap~ivity. Wlien drfetatcd seeds arc garlicred i n the iiclrl,
thr manure composi[iun s l i u~~l d I)e cor~sidererl as a cuv;lriatc, partic~~laj-ly
i n cnsrs itlhrip il i s sal-iable. Tr-ansit time 01- seed$ in the digestive tract
ncrds 11, Ilc considcrecl in l kt l ~r r rcpcri i i ~rnt s in captivity, especially i l i t is
IiighIy vai-iable xr~rl ranKes from sevcral clays to ~. \ r e~l s.
6. Examine the mechanisms by which ingested seeds have a different
germination performance from unlngested seeds
Seecl trails sucl ~ as weight, coat pcrrneahility. coat thiclille~s, textluc anrl
harrlncss niay be related tcl eltlier gcr m~i i ~t t on ~ a t c or gertniri.ll)~lity. or t o
both. For example, Ungalrc ut a! (2005) f n ~ t ~ l d lllat R~l h~rr f i . ~l ! i r nw ~ccc1.1
ingesrrrl by srp~irrels shorverl thc largest rcrl ~~ct i on in scecl coal tliickr~css
nr~cl a1 the same time had the lowrst v~abilitr: Dlte to 1x7-ialinn in rrairs
shorvn am on^ indisirlfrals wi~lrin specics uf rlispersers ancl plants (A.
Trnvesct, J . Rorlr-fguez-PC.rez all<! 13. Pii~s, tlnpuhlished r cs ~~l l s ) . the usr c)(
kiinwn seed sonrc-vs (mater-1121 plants) anrl knor*-n it~rlivirlual rlispersers will
prob~2ily shed ligllt on tEir rric.chanirms that can explain tlie tlillcier~rcs In
seccl responses ir'1t11in a sprciec.
7. Experiment with the deposltlon matrix
X cl-itical aspect of rlie influcl~ce of the frugivorrs nil SCCI ~ gcr~nillabil~ty.
which has until now h e n virtually ignoi-rd, rel;~trs to rhc ttat~ri-e of t hr
dcpositicm matrix thar sceds find themselves ill (Stiles nnrl Lt'hirc, 1986:
Jot-dano, 2000). Future stuclies !jl~oulcC recognize thar cvcds a1.r typir:<llly
rlcpositetl in faecal clumps or drirppings ancl ar e emheddcd in g mn n or
ot hrr Iaecal matter ancl ar r often competing with a ~nixturt. of scctls h-0111
one or rnt1r.e sprties. Carefi~lly designcrl sludics rtint experi n~ei ~f ~ c i t h thc.
con~po~ientsnol- this matrix will allow us to caiisitlcr e k c t s siicl~ as the
fertilizer etfrc-t, seer1 mi xi ng, the presence c> gcrmiri~tion i~ihil~itor-s andlul-
alleloc~tcmicals, anid thc arlvanr~ges trapid id or rirta!-ed ~r r i ni na t i ut ~ in thc
clump. We know vii-tuaily nothing afjour the l~elative in~poi-lance of thew
eflccts; hnu*evcl; fu1- plant species that xi-e dispersed hy lat;ge fi ~~gi voi -rs
that rlcposit large, highly rnixccl cl ~unps, ac well ;I? by srnilll nni nr~l s wit11
small clroppit~gs will1 [eh-+ ~r n mu r <l serrls, r l r es~ cfferrs Inay he \'err-
important foi- cornpal-isons of disperses etkrti\,ent.ss. All of them ~(lttlcl l>(>
cxanliriccl exper1111entaI1y 13y rt>llnrv~nji the L~t c of planted cleaned cccds ill
rliffirent tier 21 matl~iccs. t r ~ i n g difrercnt r,nmhi~i:~tinns tjf ~lcigiil>(lurs ;111rl
sced <ie~lsitieh (Loisellc, 1990). Distinguishing betwcrn allclo~~atlric ;r~rrl
direct competition is nor st~aighthr\r~arrl, hut 1I1e usr of stabilisc[l scrd
cxtracts or putiiied secondal-y trictalloIites (Cipollini and Levey, 19971 or
activ;itccl carbon r r > ;il>sorh It.acliatrs (Nilwtl11, 19g.1) tnay help sheci lig-tit CI ZI
the a c h e nleclianisn~s.
Concluding Remarks
The study of llow fnjgivorcs ~~l l l uencc the geilntnatrurt pattern< of
c~~rlozonchur~ous plant species is of great rvlcvanrr m oui- u n d e ~ rt nl l t l i n~ of'
rhrhc anitnal-pia111 inrrr.1ctiuns Train the rrtilugtcal and r vt ~l t ~t t r ~i ~asv
pcrspcctklme\. rro111 tlie plant$' >iewpnirit. ~vr neecl tn Lno~v I i t ) t ~' tile :Irrav
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