52

Journal of Zoology 289 (2013) 5259 2012 The Authors. Journal of Zoology 2012 The Zoological ociety of !on"on
Journal of Zoology
Journal of Zoology. #rint $% 0952&'3(9
The non&consu)*ti+e effects of a *re"ator on s*i"er )ites
"e*en" on *re"ator "ensity
,. -. .o/ler0 . 1ano 2 3. A)ano
!a4oratory of -cological $nfor)ation0 5ra"uate chool of Agriculture0 6yoto 7ni+ersity0 6yoto0 Ja*an
Keywords
su4lethal effects8 *re"ator*rey interaction8
anti&*re"ator strategy8 Neoseiulus
womersleyi8 Tetranychus kanzawai.
Correspondence
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A4stract
#re"ators can ha+e non&consu)*ti+e effects on their *rey 4y causing anti&
*re"ator res*onses such as changes in 4eha+iour. These effects )ay +ary /ith the
nu)4er of *re"ators0 /hich "eter)ines *er ca*ita *re"ation ris;. #re"ator "ensity
an" cue concentration ha+e 4een sho/n to affect *rey res*onses in aFuatic
*re"ator*rey syste)s8 ho/e+er0 there are fe/er tests in terrestrial syste)s. 3ere0
/e test the effects of *re"ator "ensity on *rey "is*ersal an" 4o"y gro/th in a
syste) of *re"atory )ites an" their s*i"er )ite *rey reare" on leaf *atches.
5rou*s of *rey /ere eE*ose" to a lo/ or high *re"ator "ensity le+el0 or no
*re"ators. #rey "is*erse" in the *resence of a *re"ator an" higher *re"ator
"ensity le" to greater *rey "is*ersal. 5ro/th in a"ult 4o"y siGe after )aturation
/as re"uce" in the *resence of a *re"ator0 an" this effect /as greater /ith a higher
*re"ator "ensity0 )ost li;ely relate" to a re"uction in ti)e s*ent fee"ing. -E*eri&
)ents /ere also con"ucte" to test the effects of *re"ator "ensity )e"iate" 4y
*re"atory cues alone (*re+ious *resence of *re"ators on the leaf *atch). *i"er
)ites /ere )ore li;ely to "is*erse /hen the *atch ha" *re+iously containe" a
higher "ensity of *re"ators8 ho/e+er0 there /as no effect of *re+ious "ensity le+el
on 4o"y gro/th. These fin"ings sho/ that the non&consu)*ti+e effects of a
*re"ator on s*i"er )ites can "e*en" on *re"ator "ensity an" *ro+i"e so)e
e+i"ence that che)ical cues *lay a role in this "ensity "e*en"ence. As these
changes are li;ely to affect the *re"ation rate an" *rey *o*ulation gro/th rate0
they are also li;ely to ha+e conseFuences for the *re"ator*rey "yna)ics.
$ntro"uction
#re"ators can cause a suite of 4eha+ioural0 )or*hological an"
life history changes in their *rey (Johnson0 20018 Turner0 200@8
,uFuette0 Alt/egg 2 Anholt0 20058 3o+er)an0 Aul" 2
:elyea0 20058 6alisGe/icG et al.0 20058 .ec;er)an0 Hies;i 2
.air"0 200A). Although so)e anti&*re"ator traits )ay "e+elo*
in the i))e"iate a4sence or *resence of *re"ators0 *henoty*ic
*lasticity allo/s in+est)ent in anti&*re"ator traits /hen the
4enefit is greatest an" a+oi"s *aying any associate" costs /hen
the ris; is lo/ (Agra/al0 20018 #igliucci0 20038 .enar"0 200@).
7n"erstan"ing the non&consu)*ti+e effects of *re"ators on
*rey is i)*ortant 4ecause of their i)*lications for the realiGe"
*re"ation rate an" the e)erging *o*ulation "yna)ics ($+es 2
,o4son0 19'A8 .oonstra et al.0 199'8 #reisser0 .olnic; 2
.enar"0 2005).
9osts of in+est)ent in anti&*re"ator traits can 4e a**arent
/hen *re"ators ha+e negati+e fitness i)*acts on their *rey
that arise only fro) *re"ation ris; rather than *re"ator attac;
(Te*lits;y0 #lInet 2 Joly0 20058 3a))ill0 :ogers 2 .ec;er&
)an0 200'). <or )any organis)s0 there is a tra"e&off 4et/een
anti&*re"ator 4eha+iours0 such as +igilance an" refuge use0
an" foraging (#ec;ars;y et al.0 19938 Turner0 200@8 .olnic; 2
#reisser0 2005)0 /hich lea"s to in+est)ent in anti&*re"ator
4eha+iour entailing fitness costs )e"iate" through re"uce"
energy inta;e. :ecent syntheses suggest that non&consu)*ti+e
effects of *re"ators on *rey *o*ulations can 4e as large as
effects fro) actual *re"ation (#reisser et al.0 20058 9reel 2
9hristianson0 200').
Anti&*re"ator 4eha+iour can 4e hy*othesiGe" to "e*en" on
the le+el of ris; rather than si)*ly its *resence or a4sence
(Jthreat&sensiti+e *re"ator a+oi"anceK8 3elf)an0 19'98 .arnes0
#ersons 2 :y*stra0 20028 Lrroc;0 ,anielson 2 .rin;erhoff0
200@8 Te*lits;y et al.0 20058 HalGer 2 chaus4erger0 2009)0
although there clearly )ay 4e li)its to the accuracy /ith
/hich sensory )echanis)s can assess *re"ation ris; le+el. A
clear "eter)inant of *re"ation ris; is the nu)4er of *re"ators
foraging in the +icinity0 /hich has 4een sho/n to affect the
anti&*re"ator res*onse of *rey in aFuatic syste)s (,uFuette
et al.0 20058 Te*lits;y et al.0 20058 3auGy et al.0 200A).
,ensity&"e*en"ent res*onses to *re"ators coul" arise fro) an
increase" freFuency of "irect encounters /ith the *re"ator8
ho/e+er0 li;e other infor)ation a4out their en+iron)ent0
organis)s can o4tain infor)ation a4out *re"ator *resence
,. -. .o/ler0 . 1ano an" 3. A)ano ,ensity&"e*en"ent non&consu)*ti+e effects of a *re"ator
through che)ical cues (,ic;e 2 5rostal0 20018 9ar"I 2
=illar0 200@). $n aFuatic syste)s0 anti&*re"ator traits ha+e
4een sho/n to +ary /ith the concentration of *re"ator&
"eri+e" che)ical cues (Man .us;ir; 2 Arioli0 20028 <errari0
=essier 2 9hi+ers0 200(0 200'8 <ra;er0 200'8 3a))ill et al.0
200'8 choe**ner 2 :elyea0 200').
$n the *resent stu"y0 /e test /hether si)ilar effects are
o4ser+e" in a terrestrial syste) 4y using a )ite la4oratory
syste) to in+estigate the effect of *re"ator "ensity on *rey.
#re"atory )ites ha+e 4een foun" to in"uce a range of
res*onses in their s*i"er )ite *rey inclu"ing increase" "is*er&
sal (.ernstein0 19'@8 5rostal 2 ,ic;e0 19998 L;u0 1ano 2
Ta;afuDi0 200@)0 re"uce" fecun"ity (L;u et al.0 200@8 N;alou&
"o+O0 Ze)e; 2 6rPi+an0 200A8 9hoh0 7efune 2
Ta;a4ayashi0
2010a)0 re"uce" ti)e s*ent fee"ingC)ore ti)e /al;ing (L;u
et al.0 200@8 N;alou"o+O et al.0 200A) an" use of the /e4 they
construct on the leaf surface as a refuge an" o+i*osition site
(L;u0 1ano 2 Ta;afuDi0 2003a8 !e)os et al.0 2010). .oth the
"irect *resence of *re"ators an" che)ical cues of *re"ators or
*re"ation0 for eEa)*le inDure" cons*ecifics0 affect *rey 4eha+&
iour (5rostal 2 ,ic;e0 19998 L;u et al.0 2003b8 N;alou"o+O
et al.0 200A). =uch less is ;no/n a4out ho/ these res*onses
are sensiti+e to the nu)4er of *re"ators. $n a stu"y of the
s*i"er )ite Tetranychus urticae 6och0 "is*ersal rate increase"
/ith the nu)4er of *re"ators (.ernstein0 19'@). $n another
stu"y0 the )o+e)ent of the *re"atory )ite Neoseiulus
cucumeris Lu"e)ans /as affecte" 4y the nu)4er of intraguil"
*re"ators that ha" left cues on the *atch8 fe/er re)aine" on
*atches /here there ha" 4een )ore *re"ators (9hoh et al.0
2010b).
$n the *resent stu"y0 /e stu"ie" the interaction 4et/een the
s*i"er )ite0 Tetranychus kanzawai 6ishi"a0 an" the *re"atory
)ite Neoseiulus womersleyi chicha. He eEten" *re+ious /or;
4y testing /hether a higher nu)4er of *re"ators an"Cor cues
fro) a higher nu)4er of *re"ators /oul" increase "is*ersal
an" re"uce 4o"y gro/th in this syste). The effect of *re"ators
(in ter)s of *resence or "ensity) on 4o"y siGe has not0 to our
;no/le"ge0 4een stu"ie" *re+iously in s*i"er )ites. To "eter&
)ine the associate" conseFuences0 fecun"ity an" the a)ount
of leaf "a)age inflicte" /ere also assesse".
=aterials an" )etho"s
tu"y syste)
The )ite N. womersleyi *re"ates on the *hyto*hagous s*i"er
)ite T. kanzawai. The *re"atory )ite eats all life stages of
s*i"er )ites 4ut0 li;e other s*ecialist Tetranychus *re"ators0
it *refers eggs to a"ults (<uruichi et al.0 2005). !a4oratory
*o*ulations of *re"atory )ites /ere reare" on *o*ulations of
the t/o&s*otte" s*i"er )ite T. urticae. *i"er )ite *o*ula&
tions /ere )aintaine" on *ri)ary lea+es of the ;i"ney 4ean
Phaseolus vulgaris *lace" on cotton /ool on to* of a s*onge
in a #etri "ish (9 c) "ia)eter8 1.@ c) "ee*) fille" to the to*
/ith /ater. To o4tain cohorts of 12 "ays *ost&)aturation
fe)ale T. kanzawai (hereafter *rey) for the eE*eri)ents0
a**roEi)ately @0 a"ult fe)ales /ere allo/e" to lay eggs for
2@ h0 an" the eggs /ere reare" to )aturation (at /hich *oint
fe)ales are easily "istinguisha4le fro) )ales). All )ites /ere
;e*t at 25 2Q9 an" 50 5R relati+e hu)i"ity0 /ith a
*hoto*erio" of 1(!>',.
-ffects of *re"ator "ensity
Experiment 1
To test effects on "is*ersal0 t/o&*atch syste)s /ere create"
/ithin #etri "ishes (n S 25 for each *re"ator "ensity). -ach
*atch /as a leaf sFuare (2 T 2 c))0 onto one of /hich fi+e *rey
/ere intro"uce". After 2 h0 a ti)e 4y /hich *rey ha" usually
4egun fee"ing0 the *atches /ere connecte" 4y a *arafil)
4ri"ge (2 T 2.5 c))0 an" then Gero0 one or fi+e *re"ators /ere
intro"uce" to the *atch /ith *rey. After 2 an" 2@ h0 the
nu)4ers in each *atch an" on the 4ri"ge0 inclu"ing their state
("ea" or ali+e)0 /ere recor"e".
Experiment 2
To test effects on gro/th0 fi+e *rey an" Gero0 one or fi+e
*re"ators /ere intro"uce" onto a leaf sFuare (3.5 T 3.5 c)) in
a #etri "ish (n S 30 for each *re"ator "ensity). $n each "ish0
one *rey in"i+i"ual /as selecte" as the focal in"i+i"ual an"
)ar;e" /ith a "a4 of 4lue in; on its i"ioso)a. #hotogra*hs
/ere ta;en of the focal in"i+i"uals using a "igital ca)era
secure" to the )icrosco*e eye*iece (%i;on =Z&2.0 To;yo0
Ja*an8 4inocular )icrosco*e at T50 )agnification8 ca)era
Goo) at T5) 4efore the a""ition of the *re"ator(s) an" 1 an"
3 "ays later. To )ini)iGe the ris; of the focal in"i+i"ual
4eing *re"ate"0 *re"ators /ere re*lace" /ith ne/ (an" sati&
ate") in"i+i"uals e+ery 2@ h. To )aintain a constant *rey
"ensity0 any non&focal in"i+i"ual that "ie" ("ro/ne" or *re&
"ate") /as re*lace"8 the eE*eri)ent en"e" if the focal in"i&
+i"ual "ie". At the en" of the eE*eri)ent0 3 "ays later0 the
)ites /ere )o+e" in"i+i"ually onto ne/ leaf sFuares (1.5 T
1.5 c))0 an" the nu)4er of eggs lai" after 2@ h /as counte".
The original leaf sFuares /ere scanne" 4efore an" at the en"
of the eE*eri)ent /ith a 9anon 9anocan 5@00 (To;yo0
Ja*an) at 2@00 "ots *er inch an" the i)ages sa+e" as J#-5
files for su4seFuent analysis (see "ata analysis) of the a)ount
of leaf "a)age inflicte" /hile *re"ators /ere *resent.
-ffects of *re"ator "ensity cues
Experiments 3 and 4
,is*ersal an" 4o"y gro/th eE*eri)ents /ere re*eate" 4ut
/ith *rey eE*ose" only to *re"ator cues rather than to the
i))e"iate *resence of *re"ators. #re+ious stu"ies in"icate
that s*i"er )ites can "etect che)ical cues on *atches that
*re+iously hel" *re"ators (5rostal 2 ,ic;e0 19998 N;alou&
"o+O et al.0 200A). !eaf sFuares /ere cut the "ay *rior to
each eE*eri)ent an" *lace" in"i+i"ually on cotton /ool in
#etri "ishes as in the *re+ious eE*eri)ents. Zero0 one or fi+e
*re"ators /ere intro"uce" to the sFuares0 an" sufficient
/ater /as a""e" to the #etri "ishes to create a /ater 4arrier
aroun" *atches0 )ini)iGing the ris; of *re"ators lea+ing
the) (4ecause there /as no *rey). After 2@ h0 the *re"ators
an" any eggs they ha" lai" /ere re)o+e"0 an" fi+e *rey /ere
su4seFuently intro"uce" to each *atch. $n eE*eri)ent 30 "is&
*ersal /as teste" as in eE*eri)ent 1 4y connecting the *atch
to a secon" *atch +ia a *arafil) 4ri"ge (n S 32 for each
*re"ator "ensity). $n eE*eri)ent @0 4o"y gro/th /as
assesse" as in eE*eri)ent 2 eEce*t all in"i+i"uals /ere )o+e"
onto ne/ *re"ator eE*ose" or control *atches e+ery 2@ h
(n S 30 for each *re"ator "ensity). L4ser+ations /ere also
)a"e of the *resence of any s*i"er )ite eggs on the /e4
after 1 "ay 4ecause *re+ious o4ser+ations in"icate" that eggs
are generally only lai" in the /e4 /hen there are *re"ators.
,ata analysis
To analyse "is*ersal "ata0 the *ro*ortion of in"i+i"uals
foun" outsi"e the original *atch (after 2 h an" after 2@ h)
/as analyse" using a 4ino)ial generaliGe" linear )o"el
(5!=). To in+estigate changes in gro/th0 )easure)ents
of )aEi)u) length an" /i"th of the i"ioso)a /ere ta;en
fro) the *hotogra*hs using $)age J free/are (htt*>CCrs4/e4.
nih.go+CiD)0 an" the t/o +alues /ere )ulti*lie" to create a
siGe in"eE. 5ro/th /as calculate" as the "ifference 4et/een
logarith)s of siGe 4et/een "ay 10 or "ay 30 an" the 4ase&line
siGe 4efore *re"ator intro"uction an" analyse" using analysis
of +ariance (A%LMA). !eaf "a)age /as only assesse" for
lea+es on /hich all of the original fi+e )ites sur+i+e" the
3&"ay eE*eri)ent. The scanne" leaf i)ages (fro) 4efore an"
at the en" of the eE*eri)ent) /ere con+erte" to 4lac; an"
/hite i)ages (/ith a re" filter)0 an" the leaf *eri)eter /as
selecte" using the )agnetic selection tool of A"o4e #ho&
tosho* 95 (To;yo0 Ja*an). #iEels of 0A0R grey /ere
selecte" using the colour range tool of the soft/are an" the
nu)4er of selecte" *iEels recor"e"8 A0R /as "eter)ine" as
an a**ro*riate u**er threshol" 4y co)*aring selecte" areas
/ith areas Du"ge" 4y eye to in"icate "a)age. To account for
this colour range also selecting so)e regions of un"a)age"
leaf0 such as along +eins0 /e su4tracte" the nu)4er of *iEels
selecte" on lea+es 4efore the eE*eri)ents0 /hen there /as no
s*i"er )ite "a)age0 fro) the nu)4er selecte" at the en"8
this "ifference in the nu)4er of *iEels /as then analyse"
using A%LMA. A""itional analyses on fecun"ity (sFuare" to
i)*ro+e nor)ality) an" egg *osition (analyse" as a 4inary
+aria4le8 at least one egg on the /e4 or eggs only lai" on the
leaf surface) /ere *erfor)e" using A%LMA an" a 4ino)ial
5!=0 res*ecti+ely.
$n eE*eri)ents testing the effects of the "irect *resence of a
*re"ator0 all analyses /ere 4ase" on *rey that sur+i+e"
(neither *re"ate" nor "ro/ne"). $n eE*eri)ents testing the
effect of *re"ator cues0 not all *re"ators /ere successfully
reca*ture" after 2@ h ()ost li;ely they ha" "ro/ne" in the
/ater surroun"ing the *atch or 4eca)e tra**e" in the cotton
/ool onto /hich the leaf /as *ositione"). To eEclu"e the
effect of "irect contact /ith *re"ators0 only "ata fro) re*li&
cates /here all *re"ators /ere reca*ture" /ere use". As /ell
as *re"ator "ensity0 an eE*eri)ental 4loc;ing factor ("ay) /as
inclu"e" in all )o"els. $n A%LMA0 F&tests /ere use" to test
the )ain effect of *re"ator "ensity0 /hereas t&tests /ere use"
to test )o"el coefficients8 in 4ino)ial 5!=s0 chi&sFuare"
tests /ere use" to test the )ain effect of *re"ator "ensity an"
z&tests use" to test )o"el coefficients. 9ontrasts /ere "efine"
a priori (9ra/ley0 2002) to test the co)*arisons of interest> the
"ifference 4et/een the *resence (one an" fi+e) an" the a4sence
of *re"ators an" the "ifference 4et/een one an" fi+e *re"a&
tors. All analysis /as con"ucte" using : (+ersion 2.11.08 :
,e+elo*)ent 9ore Tea)0 2010).
:esults
-ffects of *re"ator "ensity
Experiment 1: Dispersal
<e/ *rey )o+e" in the a4sence of *re"ators /hile "is*ersal
/as high in their *resence (<ig. 1a). After 2 h0 there /as a
significant effect of *re"ator "ensity le+el on the *ro*ortion of
*rey re)aining in the original *atch Uc
2
S 1A@.'0 "egrees of
free"o) (".f.) S 20 P V 0.001W0 /ith significant "ifferences
4et/een *re"ators an" no *re"ators (z S 5.1@0 P V 0.001) an"
one an" fi+e *re"ators (z S 5.250 P V 0.001). The sa)e *atterns
/ere o4ser+e" after 2@ h0 /ith greater "is*ersal in syste)s
/ith a higher nu)4er of *re"ators (all P V 0.0018 see <ig. 1).
#re"atory )ites are )uch )ore )o4ile than their *rey an"
)o+e" throughout the t/o&*atch syste). At the 2 h census0
5'.9R of *re"ators /ere o4ser+e" in the original *atch (12.'R
in the secon" *atch)0 /hereas 3(.1R /ere in the original *atch
(@A.(R in the secon" *atch) at the 2@ h census (no "ifference
4et/een one an" fi+e *re"ators0 all P X 0.2). As their )o+e&
)ent )ay ha+e cause" *rey to change *atches )ore than once
(although this /as li;ely to 4e rare /ithin 2 h)0 /e also co)&
*are" the *ro*ortion of *rey that "i" not settle in either *atch
(i.e. /ere on the 4ri"ge). The *atterns /ere consistent /ith
those a4o+e0 /ith fe/er *rey settling as *re"ator "ensity
increase". The effect of *re"ator "ensity le+el on *rey settle&
)ent /as significant after 2 h (c
2
S 9(.''0 ".f. S 20 P V 0.001)
an" 2@ h (c
2
S 51.550 ".f. S 20 P V 0.001). There /as a signifi&
cant "ifference 4et/een the effects of one an" fi+e *re"ators
after 2 h (z S 3.030 P V 0.01) although not after 2@ h (z S 1.2@0
P S 0.22)0 *ro4a4ly 4ecause *rey e+entually settle" in one
*atch in or"er to fee".
Experiment 2: Body growt! "ec#ndity and
lea" damage
*i"er )ites continue to gro/ in siGe as they fee" after )atu&
ration8 ho/e+er0 intro"ucing a *re"ator cause" s)aller
increases in 4o"y siGe (<ig. 14). #re"ator "ensity le+el affecte"
4o"y gro/th )easure" after 4oth 1 "ay (F
20A'
S 32.'A0 P V
0.001) an" 3 "ays (F
20A2
S 20.910 P V 0.001). This re"uction in
gro/th /as greater /ith fi+e *re"ators co)*are" /ith one
*re"ator (t S 2.2A0 ".f. S A'0 P V 0.05 after 1 "ay8 t S @.0A0 ".f.
S A20 P V 0.001 after 3 "ays).
After 3 "ays of eE*osure to *re"ators0 there /as an effect of
*re"ator "ensity le+el on fecun"ity in the su4seFuent 2@ h
$ig#re 1 -ffects of the nu)4er of *re"ators on> (a) *rey "is*ersal
()easure" as *ro*ortion of those ali+e not on the original *atch) after
2 h (o*en circles0 n S 250 2@ an" 25 for 00 1 an" 5 *re"ators) an" 2@ h
(grey sFuares0 n S 250 25 an" 22)8 (4) 4o"y gro/th of *rey ()easure" as
the "ifference 4et/een logarith)s of siGe ()aEi)u) length )ulti*lie"
4y )aEi)u) /i"th8 ))
2
) 4et/een 4aseline siGe an" after 1 "ay (o*en
circles0 n S 300 25 an" 2' for 00 1 an" 5 *re"ators) an" 3 "ays (grey
sFuares0 n S 290 23 an" 25) of *re"ator eE*osure. #oints are )ean
stan"ar" error. a)*les siGe +aries 4ecause re*licates /ere eEclu"e"
if all the *re"ators esca*e" or the focal in"i+i"ual "ie".
(F
20('
S 12.(90 P V 0.001)0 /ith lo/er fecun"ity of *rey that ha"
4een eE*ose" to fi+e *re"ators co)*are" /ith one *re"ator
U9.@5 0.(A ()ean stan"ar" error) +s. 12 0.A(8 t S 3.200
".f. S ('0 P V 0.01W. Also0 the fecun"ity of those eE*ose" to
*re"ators /as lo/er than the fecun"ity of those not eE*ose"
to *re"ators (13.1A 0.5@8 t S 3.'90 ".f. S ('0 P V 0.001). After
controlling for *re"ator "ensity le+el0 there /as a *ositi+e
relationshi* 4et/een 4o"y siGe an" fecun"ity (<ig. 28 F
10(A
S
11.(50 P S 0.001)0 an" this slo*e "i" not +ary a)ong *re&
"ator treat)ents ("ensity le+el T siGe> F
20(A
S 0.@00 P S 0.(A).
#atterns 4et/een an" /ithin *re"ator treat)ents are consist&
ent /ith a greater fecun"ity of in"i+i"uals that ha" a larger
4o"y siGe.
$ig#re 2 :elationshi* 4et/een fecun"ity (eggs lai" o+er 2@ h) an"
4o"y siGe ()aEi)u) length )ulti*lie" 4y )aEi)u) /i"th8 ))
2
) after
3 "ays of 4eing eE*ose" to fi+e *re"ators (soli" circles an" line)0 one
*re"ator (grey circles an" "ashe" line) or no *re"ators (o*en circles an"
"otte" line). The lines sho/ the 4ac;&transfor)e" *re"ictions fro) the
regression )o"el8 there /ere no significant "ifferences 4et/een the
fitte" slo*es for each *re"ator "ensity le+el (see results teEt).
After 3 "ays of fee"ing 4y s*i"er )ites0 the a)ount of leaf
"a)age attri4uta4le to s*i"er )ites /as greatest on lea+es
/ith no *re"atory )ites (3.9R)0 follo/e" 4y lea+es /ith a
single *re"atory )ite (2.(R) an" lo/est /ith fi+e *re"atory
)ites (1.3R). There /as a significant effect of *re"ator "ensity
le+el on the siGe of the "a)age" area (F
20@A
S 12.320 P V 0.001)
an" significantly less "a)age /ith +ersus /ithout *re"ators
(t S @.9@0 ".f. S @A0 P V 0.001) as /ell as fi+e *re"ators +ersus
one *re"ator (t S 2.190 ".f. S @A0 P V 0.05).
-ffects of *re"ator "ensity cues
Experiment 3: Dispersal
#re+ious *re"ator "ensity le+el ha" a significant effect on
*rey "is*ersal fro) the original *atch after 2 h (c
2
S @3.90
".f. S 20 P V 0.0018 <ig. 3a). A larger *ro*ortion "is*erse"
fro) *atches that ha" *re+iously containe" fi+e *re"ators
+ersus one *re"ator (z S 3.(20 P V 0.001). The sa)e tren"s
/ere o4ser+e" after 2@ h (4oth P V 0.001). $n none of the
re*licates /ithout *re"ator cues "i" fe)ales lay any eggs
in the /e4 (0C32 *atches). -ggs (at least one) /ere )ore
li;ely to 4e o4ser+e" in the /e4 in *atches *re+iously con&
taining fi+e *re"ators (12C2() than one *re"ator (2C308 z S
3.220 P S 0.001).
Experiment 4: Body growt
There /ere no significant "ifferences in *rey gro/th a)ong
*re"ator "ensity le+els after 1 "ay (<ig. 348 F
20(A
S 1.@(0 P S
0.2@). Although there /as a significant effect after 3 "ays (F
205(
S 3.A'0 P V 0.05)0 neither contrast of interest /as significant
$ig#re 3 -ffects of cues fro) "ifferent nu)4ers of *re"ators on (a)
*rey "is*ersal after 2 h (o*en circles0 )ean stan"ar" error (-)0 n S
320 30 an" 2( for 00 1 an" 5 *re"ators) an" 2@ h (grey sFuares0 n S 320
30 an" 2(). (4) .o"y siGe gro/th of *rey U)easure" as the "ifference
4et/een logarith) of siGe ()aEi)u) length )ulti*lie" 4y )aEi)u)
/i"th8 ))
2
)W 4efore the eE*eri)ent an" ti)e *oints after 1 "ay (o*en
circles0 n S 290 29 an" 1@ for 00 1 an" 5 *re"ators) an" 3 "ays (grey
sFuares0 n S 290 2@ an" '). #oints are )ean -. a)*les siGe +aries
4ecause re*licates /ere eEclu"e" if all the *re"ators /ere not
success& fully reca*ture" 4efore *rey /ere intro"uce" or the focal
in"i+i"ual "ie".
(*re"ators +s. no *re"ator> t S 1.(50 ".f. S 5( P S 0.1> one +s.
fi+e *re"ators> t S 1.3'0 ".f. S 5(0 P S 0.1A). The freFuency of
o4ser+ing at least one egg in the /e4 /as lo/er a)ong re*li&
cates /ithout *re"ator cues (z S 3.((0 P V 0.0018 1C30 *atches)
than those /ith cues (one *re"ator> 1(C298 fi+e *re"ators>
11C15)8 there /as no "ifference 4et/een one an" fi+e *re"ators
(z S 0.9(0 P S 0.3@).
,iscussion
$ncrease" in+est)ent in anti&*re"ator 4eha+iour /hen there
are )ore *re"ators is *otentially a"a*ti+e if the 4enefits of
re"uce" *re"ation ris; eEcee" the associate" in+est)ent costs.
Thus0 if an organis) can assess the nu)4er of *re"ators for&
aging near4y0 its anti&*re"ator 4eha+iour )ay o*ti)ally 4e
sensiti+e to *re"ator "ensity (3elf)an0 19'9). =any stu"ies
ha+e in+estigate" the effects of *re"ator cue concentration on
*rey in aFuatic syste)s (e.g. <errari et al.0 200'8 <ra;er0 200'8
choe**ner 2 :elyea0 200'8 3a))ill et al.0 200'). $n the
*resent stu"y0 the effect of *re"ator "ensity on *rey 4eha+iour
/as teste" in a )ite la4oratory syste) in /hich *re"ators ha+e
4een *re+iously sho/n to "ecrease ti)e s*ent foraging an"
*ro)ote "is*ersal (L;u et al.0 200@). Lur fin"ings su**ort the
hy*othesis that the anti&*re"ator 4eha+iour of s*i"er )ites is
sensiti+e to *re"ator "ensity.
9onsistent /ith a *re+ious stu"y on a closely relate" s*i"er
)ite (T. urticae8 .ernstein0 19'@)0 the *ro*ortion of *rey that
"is*erse" increase" /ith the nu)4er of *re"ators *resent. He
also sho/e" that *rey 4o"y gro/th can 4e affecte" 4y *re"a&
tor "ensity. #rey gre/ less in the *resence of a *re"ator0 an"
this re"uction in gro/th /as greater /ith a higher *re"ator
"ensity. After )aturation0 s*i"er )ites continue to gro/ in
siGe /hen they fee" an" so these changes in siGe )ay reflect
changes in *rey fee"ing 4eha+iour. :e"uce" siGe in the *res&
ence of *re"ators has 4een o4ser+e" in )any organis)s an"
has usually 4een eE*laine" through *re"ator&sensiti+e forag&
ing (#ec;ars;y et al.0 19938 Turner0 200@). A *re+ious stu"y on
this s*i"er )ite foun" increase" use of the /e4s0 sus*en"ing
in"i+i"uals a4o+e the leaf surface0 /hen a *re"ator /as
*resent0 /hich re"uce" the *ro4a4ility of 4eing attac;e" (L;u
et al.0 2003a)8 ho/e+er0 this 4eha+iour is li;ely to restrict
fee"ing. Although /e use" a coarse techniFue to assess leaf
"a)age0 the *atterns suggeste" that there /as less "a)age on
leaf *atches /ith *re"ators0 *articularly a higher nu)4er of
*re"ators. Thus0 a re"uction in fee"ing ti)e is also su**orte"
4y the change in esti)ate" leaf "a)age. .ecause assi)ilation
efficiency of ingeste" foo" also affects gro/th an" )ay change
un"er *re"ation ris; (e.g. to;s et al.0 2005)0 it cannot 4e rule"
out that re"uce" assi)ilation efficiency contri4ute" to the
s)aller gro/th of *rey.
Lne *ossi4le eE*lanation of the "ensity "e*en"ence is
that an increase" freFuency of "irect encounters /ith *re"a&
tors0 causing "istur4ance to *rey fee"ing0 le" to a greater
re"uction in fee"ing. To in+estigate /hether che)ical cues
coul" also *lay a role0 /e teste" /hether "ensity&"e*en"ent
res*onses e)erge" if *rey /ere eE*ose" in"irectly to *re&
"ators through che)ical cues they left on a *atch. #re+ious
stu"ies ha+e confir)e" that s*i"er )ites can *ercei+e
such cues (5rostal 2 ,ic;e0 19998 N;alou"o+O et al.0 200A)0
/hich are )ost li;ely )eta4olic /aste *ro"ucts. He foun"
that a greater *ro*ortion of *rey "is*erse" fro) *atches that
ha" *re+iously containe" a higher nu)4er of *re"ators.
There /as no effect of cues on *rey gro/th0 4ut the o4ser&
+ation of eggs 4eing lai" in the /e4 in"icates that cues /ere
"etecta4le.
Marious cues are *otential in"icators of *re"ation ris;8
so)e cues are e)itte" 4y the *re"ator0 /hereas others are a
conseFuence of its interactions0 for eEa)*le inDure" *rey
(,ic;e 2 5rostal0 20018 Lrroc; et al.0 200@). o)e cues )ay
4e )ore relia4le in"icators of ris;0 *articularly those only
*erce*ti4le /hen the *re"ator is near4y. $n our eE*eri)ent0
the che)ical cues fro) /aste *ro"ucts lai" 4y *re"ators *re&
+iously on the *atch are li;ely to in"icate a lo/er le+el of
ris; than those "etecte" in the i))e"iate *resence of a
*re"ator 4ecause such cues re)ain for a *erio" of ti)e after
the *re"ator has left the *atch. The relationshi* 4et/een cue
age0 "egra"ation an" "etection has yet to 4e esta4lishe" 4ut
longer li+e" che)ical cues )ay 4e less relia4le in"icators of
i))e"iate ris; (.arnes et al.0 2002). As suggeste" 4y the
relationshi* 4et/een 4o"y siGe an" fecun"ity0 re"uce" ti)e
s*ent foraging )ay carry costs in ter)s of fecun"ity. .y con&
trast0 /hether "is*ersal is costly "e*en"s on the a4ility to
fin" a ne/ leaf *atch near4y. Thus0 +ariation in cue relia4il&
ity an" costs of in+est)ent in "ifferent anti&*re"ator 4eha+&
iours )ay eE*lain /hy *re"ator *resence0 an" not cues fro)
*re"ators *re+iously on the *atch0 re"uce" gro/th. Lther
e)*irical stu"ies ha+e also foun" that "ifferent cues0 or cue
concentrations0 sti)ulate "ifferent anti&*re"ator res*onses
(3ar+ell0 199'8 Man .us;ir; 2 Arioli0 2002). He hy*othesiGe
that "ifferent le+els of *ercei+e" *re"ation ris; can lea" to
"ifferent anti&*re"ator res*onses accor"ing to their costs0
/ith )ore costly 4eha+iours 4eing sti)ulate" 4y )ore reli&
a4le cues.
Lur fin"ings suggest that the non&consu)*ti+e effects of a
*re"ator can "e*en" on *re"ator "ensity8 ho/e+er0 there are
a nu)4er of li)itations to our conclusions. <irst0 only t/o
*re"ator "ensities /ere teste". .ecause of the s)all leaf area
relati+e to the high )o+e)ent ca*acity of the *re"ator0 *rey
)ost li;ely encountere" a *re"ator /hen there /as either
one or fi+e *resent on the *atch. 3o/e+er0 cues fro) a single
*re"ator )ay not 4e "etecte" if cues are reFuire" to 4e
a4o+e a threshol" concentration for *rey to "etect the). As
the "ifference 4et/een the cues of Gero an" one *re"ator on
"is*ersal /as s)all0 there /as so)e in"ication that cues
fro) one *re"ator /ere less li;ely to 4e "etecte". $n+estiga&
tion of the sha*e of the continuous relationshi* 4et/een
*re"ator "ensity an" *rey res*onse coul" gi+e further insight
into the sensory ca*a4ility of *rey for *re"ator "etection
an" /oul" strengthen the e+i"ence for *re"ator "ensity&
"e*en"ent *rey res*onses. econ"0 /e in+estigate" the effects
of the a""ition of one s*ecies only. 9o)*etiti+e s*ecies can
4e eE*ecte" to ha+e si)ilar "ensity&"e*en"ent effects on "is&
*ersal an" gro/th 4ecause they use the sa)e resources.
3o/e+er0 it is *ossi4le that other non&*re"atory s*ecies also
affect "is*ersal an" gro/th si)*ly 4y causing "istur4ance to
foraging )ites8 these effects )ay +ary accor"ing to traits
such as 4o"y siGe an" acti+ity le+el. Thus0 it cannot 4e
assu)e" that these effects are restricte" to *re"ators0
although /e )ay eE*ect the effect siGe to "iffer. Thir"0
further eE*eri)ents are necessary to "eter)ine ho/ the
res*onses co)4ine in a real lan"sca*es8 for instance0 /hether
the arri+al of a *re"ator si)*ly "elays *rey fee"ing an"
s*rea"s out su4seFuent *lant "a)age /ithout affecting
s*i"er )ite fecun"ity.
tu"ies )easuring the functional res*onse of *re"ators
suggest that there )ay 4e interference at high *re"ator
"ensity (A4ra)s 2 5inG4urg0 2000). Lur results suggest that
*re"ators )ay face a for) of J"etection interferenceK /hen
foraging on a *rey *atch /ith cons*ecifics. #rey are )ore
li;ely to "etect an"Cor in+est in anti&*re"ator 4eha+iour /hen
there are )ore *re"ators0 /hich can 4e *re"icte" to ha+e
;noc;&on effects on *re"ation success. A secon" i)*lication
of these results is that changes in *rey 4eha+iour )ay lea" to
casca"ing effects on lo/er tro*hic le+els (ch)itG0 .ec;er&
)an 2 LK.rien0 199A8 3li+;o 2 :y*stra0 20038 HalGer 2
chaus4erger0 2009)0 /hich0 in this stu"y syste)0 lea"s to less
*lant "a)age 4y *hyto*hagous )ites /hen *re"atory )ites
are *resent. $f these *rey res*onses affect *re"ation rate0 they
are also li;ely to ha+e i)*lications for the *re"ator*rey
*o*ulation "yna)ics. $ncrease" "is*ersal an" re"uce" ti)e
s*ent foraging 4y *rey )ay re"uce *re"ation success at high
*re"ator "ensity8 therefore0 /e can s*eculate that they )ay
ha+e sta4iliGing effects on the interaction.
Ac;no/le"ge)ents
This research /as fun"e" 4y a Ja*an ociety for the #ro)o&
tion of cience short&ter) *ost&"octoral fello/shi* to ,.. He
than; =asahiro Lsa;a4e an" )e)4ers of the !a4oratory of
-cological $nfor)ation at 6yoto 7ni+ersity for "iscussion as
/ell the referees for co))ents on the *a*er.
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