Download The Interplay of Biotic and Abiotic Factors in a Semiarid

The Interplay of Biotic and Abiotic Factors in a Semiarid Chilean Mammal
Assemblage: Results of a Long-Term Experiment
Peter L. Meserve; W. Bryan Milstead; Julio R. Gutiérrez; Fabian M. Jaksic
Oikos, Vol. 85, No. 2. (May, 1999), pp. 364-372.
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OIKOS 85: 364-372. Copenhagen 1999
The interplay of biotic and abiotic factors in a semiarid Chilean
mammal assemblage: results of a long-term experiment
Peter L. Meserve, W. Bryan Milstead, Julio R. Gutihrrez and Fabian M. Jaksic
Meserve. P. L.. Milstead. W. B.. Gutierrez. J. R. and Jaksic. F. M. 1999. The
interplay of biotic and abiotic factors in a semiarid Chilean mammal assemblage:
results of a long-term experiment. - Oikos 85: 364-372.
Since early 1989, we have conducted a large-scale ecological manipulation in a
semiarid thorn scrub community in north-central Chile. We have excluded vertebrate
predators (raptors and mammalian carnivores), and larger small mammal herbivores
competitors (i.e., degus, Octodon clegus) from replicated 0.56-ha plots, and monitored
small mammal population and plant responses over more than ten years. Repeated
measures ANOVAs on minimum number known alive (MNKA) estimates of small
mammals for a six-year period (1990- 1996) spanning an El Nifio event in 1991- 1992
showed strong responses of some species to predator exclusions (e.g.. 0 . clegus:
Darwin's leaf-eared mouse. Phylloris tft~rivini:the chinchilla-rat. Ahroconiu hennetti).
However. responses varied in time with siguificant effects during pre-El Nitio
(1990-1992) and El Nitio (1992-1994) periods (i.e.. 0 . degus). or pre-El Nifio and
post-El Nitio (19941996) periods (P.rkrri~.itii.A . hetinetti). Other species showed no
responses to predator exclusions (e.g.. olivaceous field mouse. Akotfotz olirrrceus;
long-haired field mouse. Abrothrih- longiyili.~;long-tailed rice rat. Oliporj~zotnyslongii,uurlrrr~rs).Some effects of competitor (degu) exclusions were detected (e.g., A.
hennetti during the El Nitio and post-El Nirio periods: 0 . longictrutlutus during the El
Nifio). "Top-down" factors (i.e., biotic interactions) appear to have greater effects on
0 . deg~is)which persist in the thorn scrub. Other
"core species" (i.e.. P. (Ic~r~cini.
species (e.g.. ' 4 . 1ongipili.r. 0 . longicrr~iclirtus)are transitory residents or "opportunistic" with lesser effects of biotic interactions. and their populations may be controlled
by source-sink dynamics. All species had strong responses to the 1991-1992 El Nifio
indicating primary control by "bottom-up" factors.
P. L. Meserccz and W . B. Mihtead: Dept of'Biologica1 Sciences. ~VortlrernIllinois Ckic..
De Kulb, IL 60115. U.S.A.: ([email protected]~r).- J. R.Gutiirre:: Depczrtummto c/e
Biokogiu. I.rtli~e~.sid(zd
de La Serenu. Cusillu 599, La Serentr, Chile. - F. M . Jaksic.
Departiimetito de Ecologia. P. Unicersichd Curciliccr tfe Chile, Cusilln 114-0. Suntiago.
Chile.
Debates on the role of density-dependent vs density-independent population regulation and that of biotic vs
abiotic factors have been largely parallel (e.g.. Andrewartha and Birch 1954. Dunson and Travis 1991),
but not independent. Biotic interactions must be viewed
against a background of constantly changing abiotic
conditions (e.g., Wiens 1977, 1986, 1989. Wiens et al.
1986), and environmental fluctuations and harshness
per se do not preclude their importance (Chesson and
Huntley 1997). An extension of this debate has been the
Accepted 21 January 1998
Copyright % OIKOS 1999
ISSN 0030-1299
Printed in Ireland all rights reserved
-
degree to which populations at one trophic level are
controlled by their consumers ("top-down control") or,
alternatively. by abiotic factors which influence resources constraining producers and or their consumers
("bottom-up control": Power 1992). Here. various hypotheses have emerged. For example, the "HSS" hypothesis of Hairston et al. (1960) predicts "top-down"
control of herbivores by their consumers. Plants, detritivores, and predators in turn are limited by available
resources. Predator removal should lead to increases by
herbivores (but not granivores; Slobodkin et al. 1967),
and strong effects of the former on plants. Their absence also could lead to strong negative effects on
granivores as herbivores increase and graze down vegetation. An extension of this. the exploitation ecosystems
hypothesis ("EEH"), predicts that below some productivity threshold. herbivore biomass is insufficient to
support predators on them, and herbivores have weak
effects on plants. Under these conditions, predatol
exclusions should have little effect since they are relatively unimportant: in more productive environments or
periods. predators can exert strong effects on herbivores when they reach higher densities due to increased
productivity (Oksanen et al. 1981. Oksanen 1992).
Purely "bottom-up" hypotheses (e.g.. White 1978.
Hunter and Price 1992) predict that all trophic levels
are essentially limited by available resources (i.e..
"donor-controlled": Polis and Strong 1996). and that
"top-down" interactions (i.e., predation. herbivorq) are
relatively unimportant. Thus. predator or herbivore
exclusions would result in little or no effects on consumers or primary producers at loner trophlc levels.
Although much uork has been done on these hypotheses in aquatic systems. terrestrial sqstems have
received less attention perhaps because of the large
spatial and temporal scales involved. and or the
difficulty of manipulations. Experiments tend to focus
on single interactions (i.e.. competition. predation. herbivory) with some notable exceptions (e.g.. McNaughton 1976, Davidson et al. 1984. 1985. Brown et
al. 1986, Guo et al. 1995. Krebs et al. 1995. Ostfeld et
al. 1996, Valone and Brown 1996).
Arid systems offer unusual opportunities to investigate these hypotheses because of high variability of
rainfall both within and between years. In the Western
Hemisphere. arid regions often have high rainfall associated with El Nifio Southern Oscillation (ENSO)
events. leading to shifting conditions in which "topdown" (primarily biotic) vs "bottom-up" (primarily
abiotic) factors may have "primacy" (sensu Hunter and
Price 1992. Power 1992). However. the small temporal
and spatial scale of most field experiments (Sih et al.
1985, Kareiva and Anderson 1988. Tilman 1989) results
in difficulty distinguishing the relative importance of
abiotic vs biotic factors in long-tern~community organization. Large-scale studies (particularly long-term
ones) are often necessary to demonstrate the subtle
interplay of biotic and abiotic factors. They also offer
opportunities for integrating information from different
organizational levels ( L e ~ i n1992) and the study of slou
phenomena, rare events. subtle + complex processes
(sensu Franklin 1989, Pickett 1991). and hidden processes in the "invisible present" (Magnuson et al. 1991).
Since early 1989, we have conducted a large-scale
manipulation in a semlarid locality in north-central
Chile with primary focus on the importance of biotic
interactions, specifically vertebrate predation, interspe-
cific competition, and herbivory, on the small manlmal
assemblage and plants using a "press" approach (sensu
Bender et al. 1984). Initial results (e.g., Meserve et al.
1993a. b, 1996, Gutierrez et al. 1997) established the
importance of biotic interactions on several small mammal and plant species. However. populations of small
mammals and plants in the Chilean semiarid region
also show strong fluctuations. particularly in response
to high rainfall during El Niiio events (e.g.. Fulk 1975.
Pearson 1975. Pefaur et al. 1979. Fuentes and Campusano 1985. Dillon and Rundel 1990. Jimenez et al.
1992, Meserve et al. 1995. Gutierrez et al. 1997). In a
sense. El Niiio events are natural "pulse" experiments
that alter the role of biotic vs abiotic factors. Here. we
analyze their importance in a small mammal assemblage during El Nifio and non-El Niiio periods.
Study area and methods
Study site
The study site is located in Fray Jorge National Park.
Chile (71°40'W, 30'38's: IV Region) 100 km S La
Serena and 350 km N Santiago near the coast. This
10 000-ha World Biosphere Reserve is primarily semiarid thorn scrub but also has isolated fog forests on
coastal ridges that have been protected from grazing
and disturbance since 1941. The flora of the lower
elevational scrub zone includes spiny drought-deciduous and evergreen shrubs and understory herbs on a
predominantly sandy substrate (Muiioz and Pisano
1947. Gutierrez et al. 1993a. b). The climate is semiarid
mediterranean with 90% of the precipitation falling in
winter (May-September): summer months are warm
and dry. Mean annual precipitation is 85 mm. but
coastal fog and high relative humidity result in dew
ameliorating aridity. After a normal year in 1989 (89
mm), and a dry one in 1990 (32 mm). El Niiio's in
1991-1992 resulted in 233 mm and 229 mm. respectively: I 9 9 3 1 9 9 6 were normal to below normal (77, 35.
54. and 70 mm. respectively).
The small mammal assemblage in the thorn scrub
includes the herbivorous 120-150 g degu (Octodon
d?gus (Molina)) and uncommon 150-250 g chinchilla
henr~etri Waterhouse), and several
rat (Abvoco~~~u
smaller (20-80 g) species such as the omnivorous olivaceous field mouse (Akodorl olit~aceusWaterhouse), the
granivorous long-tailed rice rat (O/igo~.zolnj,~
[Orj.z o ~ ~ ~ longicaudutus
j.s]
(Bennett)). the insectivorous longhaired field mouse (Ahrothris [Akodon] lor~gipilis
(Waterhouse) and mouse opossum (T!~ylumj.s [Marr?~osa] rlegnns (Waterhouse)). and the herbivorousgranivorous leaf-eared mouse (Phj.llotis durwini
(Waterhouse) (Meserve 1981 b). Rare species include the
coastal degu (OctoOon lurz~itusOsgood). mole mouse
(Cllrlernj~s rnegalorzj..~ (Waterhouse)). and fossorial
(i.e., time) were also examined. Statistical significance
was set at P 2 0.05, but values o f ( a = 0.05-0.10 were
considered suggestive o f treatment effects given high
variance o f changes over time. Grids were randomly
assigned, and no significant among-treatment differences were found in densities o f the principal species or
vegetative cover at the start o f the experiment when
exclosures were being installed (March-May 1989).
Our hypothesis was that the relative importance o f
biotic interactions (i.e.. interspecific competition, and
vertebrate predation) varied in relation to numbers o f
Methods
putative strong interactors in the population and that
In early 1989, we established 16 75 m x 75 m (0.56 ha) this was reflected by their numerical responses to the
grids in the valley. The design o f the project (see 1991 - 1992 El Nifio. Thus, degus. a putative competiMeserve et al. 1993a. b 3 1995. 1996) includes four grids tor. which had a delayed demographic response increaseach with: a) low (1.0 m high) 2.5-cm mesh fencing ing above mean baseline densities in September 1992,
buried 40 cm with 5-cm diameter holes at ground level and declining below those levels in mid-1994 (Meserve
to allow all small mammal + predator access (hence- et al. 1996). should have had their strongest impact on
forth + D + P): b ) 1.8-m fencing buried 40 cm, with other species from mid-1992 through mid-1994. SimiI - m overhangs, polyethylene mesh (ca 15 cm diameter) larly. vertebrate predator numbers exhibited a delayed
netting overhead. and holes at ground level to exclude response increasing in the "nonbreeding season"
predators, but allow small mammal access (including (March-August) 1992, and declining after the "breeddegus; + D - P): c) low fencing similar to a ) but ing season" (September-February) o f 1993-1994 (Jakwithout holes to allow access by predators and most sic et al. 1997). Therefore. after conducting
small mammals but exclude degus ( - D + P): and d ) rmANOVAs on the total data set for each species
high fencing without holes. but with overhangs and between September 1990 and August 1996 (IY = 72 mo.;
netting to exclude both predators and degus ( - D "overall analysis"), we reanalyzed data for three twoyear periods (24 mo each) for September 1990-August
- P).
W e live-trapped small mammals for four nights per 1992 ("pre-El Niiio"). September 1992-August 1994
month on each grid (5 x 5 stations, 15-m interval, two ("El Niiio"). and September 1994-August 1996 ("posttraps station) and marked all captured animals with ear El Niiio"). As noted above. these periods correspond to
tags or leg bands. Traps were left open continuously times when both degu and predator densities were low,
during winter months and checked twice daily; during high, and then low in the study area. as well as "wet"
warmer summer months. they were closed after the and "dry" seasons (Meserve et al. 1996) and predator
morning check, reopened at mid-afternoon, and seasons used for analyses o f their diets and abundance
rechecked at dusk. Monthly trappability was high for (Jaksic et al. 1997).
the principal species ( > 90%)) except for 0 , ~iegus
Statistical inferences from rmANOVAs were based
(x = 69.09 Ifr 2.14[SE]'i/0)
enabling use o f minimum num- on Type 111 sum-of-squares and all P values for withinber known alive ( M N K A )estimates. Methodologies for subject analyses were Huynh-Feldt adjusted which cormonitoring plant changes, and predator activity, abun- rects for deviations in the sphericity assumption o f the
dance and diet were described elsewhere (Gutierrez et variance-covariance matrix (von Ende 1993). W e veral. 1993a. b, 1997, and Jaksic et al. 1993. 1997. ified the A N O V A assumption o f homogeneity o f varirespectively).
ances by visual inspection o f Studentized plots o f
residuals against predicted values generated by PROC
GLM (SAS 1990): none o f the 28 rmANOVAs yielded
obvious deviations from expected random scatter plots
Analyses
(Stevens 1992). and no transformations were deemed
The experiment is a 2 x 2 factorial design with grids necessary.
randomly assigned to treatments (i.e.. competition~herbivory [presencetabsence o f degus],and predation [presence,'absence o f carnivores + raptors]). For small
mammal responses, repeated measures analysis o f variResults
ance (rmANOVA, PROC G L M : SAS 1990. Potvin et
al. 1990, von Ende 1993), and M N K A estimates o f the Through June 1997. 121 517 captures o f 18 390 individprincipal species were used. Between-treatment (main) uals o f nine species o f small mammals were recorded
effects were predation (for degus), and predation and during approximately 559 000 trap-nights over 100
competition (for non-degus); within-treatment effects months o f study. During the 72 months analyzed here.
coruro (Spalacopus cyanus (Molina)).The most important small mammal predators are owls (Speotyto cunicularia, Tyro albu, Bubo cirginianus, and Gluucidium
nanurn), and culpeo foxes (Pseudalopex culpaeus
(Molina); Jaksic et al. 1992. 1993. 1997). Predator
numbers in the park are unusually high because it is
one o f the few undisturbed areas o f semiarid scrub in
the north-central region o f Chile.
a total o f 110 004 captures o f 15 844 individuals occurred (90.5% and 86.2% o f captures and individuals,
respectively). Trap success varied from 1-2% during
1990 and 1996 to > 100%1(due to multiple captures in
the same trap) with up t o 4600 captureslmo during and
after El Nifio years.
Predation affected the abundance o f Octodon drgus
overall (F,., = 7.42. P = 0.034). The effect o f predation
was pronounced during the pre-El Niiio (F,,,= 6.53.
P=0.043), and marginally nonsignificant in the El
Niiio (F,., = 5.69, P = 0.054), but not significant in the
post-El Niiio (F,,,= 0.18, P = 0.689). There were significant within-treatment interactions between time and
predation overall (F7,,,,, = 4.44. P = 0.023). during the
pre-El Niiio (F,,,, = 2.42, P = 0.021). and El Niiio
=
P = 0.013). but not during the post-El
(F23,1384.62.
= 1.61. P = 0.169: Fig 1 ). indicating that
Niiio (F23,138
predation was changing in intensity during these periods. Although absolute numerical differences between
predated and non-predated populations during the El
Niiio were greater than during the pre-El Niiio, percentage differences were smaller (Fig. 1). Degus had
delayed numerical responses increasing in September
1992 nearly 18 m o after the start o f increased rainfall in
1991-1992 (Meserve et al. 1995; Fig. 1).
Predation also affected Phyl1oti.c clurlcini overall
( F , , , 2= 5.94. P = 0.031). but unlike 0 . degus, it was
highly significant in the pre-El Niiio (F,,,?= 13.86. P =
0.003), and the post-El Niiio ( F , , ] =
? 23.03, P = 0.001).
but not during the intervening El Niiio; the magnitude
o f this effect. however, was small (Fig. 1 ) . There were
significant time x predator interactions for all time periods (overall: F7, j,
= 2.20, P = 0.017: pre-El Nifio:
F23,27h
= 2.24, P = 0.015: El Niiio: F23,27h
= 1.89, P =
0.043; post-El Niiio: F,,
= 6.49. P = 0.001). Predator x degu interactions were marginally nonsignificant
overall. and during the El Niiio (F,,,?= 4.24. P = 0.062,
and F,,,>= 4.02. P = 0.068. respectively) as was a
=
time x degu interaction during the El Niiio (F23,27h
1.73. P = 0.068). P. durwini had regular annual fluctuations in abundance regardless o f drought
conditions
and major increases occurred primarily during dry
/ PRE-EL NINO 1
ELNlRO
I POST-EL NINO
(summer) months due to recruitment (Meserve and Le
Boulenge 1987. Meserve et al. 3995: Fig. 1 )
0 0
Octodon degus
There were no effects o f predation or competition on
numbers o f Akodoiz olirmcrus overall or by two-year
periods, nor any significant within-treatment interactions (Fig. 1). This species showed the strongest and
most rapid response to the 1991 - 1992 El Nifio with
increases during both the wet and dry seasons, and a
sharp decline after 1993 (Fig. 1 ) . Similarly. there were
w
no effects o f predation or competition on numbers o f
V)
I Phyllotis d a n v ~ n ~
? loo
Abrotlzris longipili.~. Although trends are suggestive o f
higher numbers in - D + P grids (Fig. 2). this species
was generally low in abundance and between-grid variation was high. thus yielding nonsignificant betweentreatment effects. Marginally nonsignificant, and
significant within-treatment interactions (time x predation) were present overall ( F7,,,, = 2.19. P = 0.057).
and for the El Niiio (F2',,,:, = 2.10. P = 0.036),
I
/ Akodon olivaceus
t + Degus + Predators
respectively.
2 100
-0- + Degus - Predators
Results for Oligorj~zornj,slongicaudatus, Abrocomrr
t - Degus + Predators
bnzrzrtti. and Tlzylaniys eleguns were interpreted cau-0- - Degus - Predators
tiously due to generally low numbers and or large
fluctuations in abundance. Numbers o f 0. longicaudatu.r showed a significant effect o f competition during the
El Niiio only (F,.,:= 8.36. P = 0.014). although numerical differences between treatments were small (Fig. 2).
This species is highly nomadic with large between-year
D
J
D
J
D
J
D
J
D
J
D
J
oscillations in northern semiarid localities (Pefaur et a].
1990
1991
1992
1993
1994
1995
1996
1979, Fuentes and Campusano 1985. Meserve et al.
Fig. 1. Population trends of Octodon degus (top). Pl~yllotis
clarn,ini (middle) and Akodon olicaceu.~(bottom) during Sep- 1995).
A. bcnr~ettihad significant predation effects overall
tember 1990 through August 1996 (standard errors omitted for
clarity). Treatments indicated by symbols and labels. Analyzed
( F l , l=
z 7.55, P = 0.018). and during the pre-El Niiio
periods indicated by bars on top corresponding to pre-El
( F , , 1=
2 7.28, P = 0.019). and post-El Niiio ( F = 8.38,
Nifio, El Nifio, and post-El Nifio (see text for exact months).
P = 0.013) (Fig. 2). It also had marginally nonsignifiSymbols "J" and "D" on abscissa correspond to June and
December for each calendar year.
cant competitor effects overall ( F , , , ,= 3.51. P = 0.086).
,,
,,
,-,
-
f
~
~
,,,,
loo
i
Abrothrix longipilis
Oligotyzornys longicaudatus
2
f
9
~
+ + Degus + Predators
-0-
I0i
+ Degus - Predators
t
-
-0-
- Degus
Degus +Predators
-
Predators
I
Abrocoma bennetti
tive. Population trends suggested two- to three-year
cycles in abundance; peaks occurred in early-mid 1990,
1992. 1994 and 1997.
Changes in numbers of small mammals with the
strongest predation effects (0. degus. P. darwini, A.
hennetti) on control ( + D + P) grids were contrasted
with their proportions in the diets of three predators
(Bubo cirginianus. Tvto alba. and Pseud~rlopexculpaeus)
at the site during the six years (Fig. 3: data from Jaksic
et al. 1997 and unpubl. data: see Fig. 2 for A. hennetti
population trends). During the pre-El Niiio. the owls
utilized 0. degus and P. clnr~c,iniextensively: A. bennetti
was also consumed by the fox P. culp~~eus
(Fig. 3).
Concurrently. significant main treatment effects of predation were detected on all three species. Proportions of
P. rkir~vinirose in the diets of all predators as their
numbers increased in the pre-El Nifio (Fig. 3). During
the El Niiio. proportions of 0. degus increased in the
diets of all predators, and a marginally nonsignificant
predation effect was detected on this species although
Bubo v~rglnranus
60
40
D
J
D
J
D
J
D
J
D
J
D
J
20 O
I
L
b..
-
A
,
A
Fig. 2. Population trends of Ahrothrr.~Iorzgipilis (top). Oligory:orn>.J 1ongicaudutu.r (middle), and Ahrocornu hennetti (bottom) during September 1990 through August 1996 (standard
errors omitted for clarity). Treatments indicated by symbols
and labels. Analyzed periods indicated by bars on top corresponding to pre-El Nifio. El Nilio, and post-El Nitio (see text
for exact months). Symbols "J" and "D" on abscissa correspond to June and December for each calendar year.
Populations were higher in degu-exclusion grids during
the El Niiio ( F , . , ?= 4.49. P = 0.056), and post-El Niiio
periods (F,.,?= 4.40. P = 0.058). There were marginally
nonsignificant to highly significant time x predation (El
Niiio: F23.2,h= 1.54. P = 0.096). and time x competitor
interactions (overall: F,,.,52 = 3.05. P = 0.001: pre-El
= 3.19,
Niiio: F23,276= 1.58. P = 0.091; El Nifio: F,
P = 0.001). Only this species had significant time x
predator x competitor interactions (overall: F,,,,,, =
1.62, P = 0.093: pre-El Niiio: F23.27h= 1.79, P = 0.046;
El Niiio: F2,,,,, = 1.77. P = 0.044) indicating that
predators and degus were influencing A. be~znertinumbers in a complex manner.
T. elegans showed marginally nonsignificant competitor effects overall ( F , , , ?= 4.10, P = 0.066). and during
the El Niiio (F,.,?= 3.70. P = 0.078) with numbers being higher on degu-access grids. However. numbers
seldom exceeded 8- 10 individuals grid. trappability
was low, and population trends were complex. thus
rendering interpretation of biotic interactions specula-
,,,,,
'
,,
"
100
1
Pseudalopex culpaeus
1
?RE-EL
D
1990
NINO
1
ELNlW
1
POST-EL NINO
J
D
J
D
J
D
J
D
J
D
1991
1992
1993
1994
1995
1I
J
1996
Fig. 3. Proportions of small mammal prey (Octodon clegus.
Plz~llotis drrrnini and Ahroconzci hennetti) in diets of Bziho
uir-ginianus, Tj.to ulba, and Pseutkalope.~cull,aeus during September 1990-August 1996 (pre-El Nifio. El Nifio. and post-El
Nifio periods labeled on top; see text for exact months), and
population trends for Octodon degus and Phj~lloti~
durn,ini on
P) during the same period (bottom).
control grids ( D
Population trends for A . hrnnetri omitted, but see Fig. 2,
bottom.
+
+
its magnitude was smaller than during the pre-El Niiio
(Fig. 1). Finally, during the post-El Niiio when 0.
degus numbers were declining, highly significant predation effects were detected on both P. darwini and A.
hennetti, but not 0. degus. when the former two species'
proportions in predator diets began to increase again
( A . berznetti in B. rirginianus and T. nlba; P. darlt.ini in
B. z)irginianus and P. culpaeus: Fig. 3). These results
suggest switching among prey concomitant with intrinsic responses of small mammals to the 1991-1992 El
Niiio.
Discussion
Our analyses provide further support for the importance of vertebrate predation on numbers of three
. . durwini, and A.
species of small mammals ( 0 . d e g u ~ P
bennetti) in Fray Jorge. We previously noted important
effects of predation on numbers and survival of these
species during 1989-1994 with seasonal and yearly
analyses (Meserve et al. 1993b. 1996). Other species
such as A . olicaceus, T. elegans, 0. longicaudatzls. and
A. longipilis showed no importance of predation on
their numbers although there were a few time x predation interactions (i.e., A . longipilis). These species are
distinctly lower in predator preference relative to others
(Jaksic et al. 1993, 1997). Important survivorship and
behavioral effects of predators on 0. clegus and other
small mammal species have also been found (e.g..
Vasquez 1994, 1996. 1998. Lagos et al. 1995, Meserve et
al. 1996. P. L. Meserve and J. A. Yunger. unpubl.
data). Thus. predation may be manifested not only by
numerical changes, but also changes in behavior. survivorship and other aspects.
The evidence for competition effects is much weaker.
Only one significant deg; competition effect was found
on 0. longiccrudutus during the El Niiio period, and
marginally nonsignificant effects overall, and during the
El Niiio and post-El Niiio; there were also marginally
nonsignificant con~petitioneffects on A. bennetti. Both
findings are intriguing. 0. lorzgicaerdatus, a nocturnal.
bipedal granivore which uses open, more risky foraging
environments (Meserve 1981b. Simonetti 1989, Vasquez
1996) would seem an unlikely competitor with herbivorous 0. degus. However, under bofh "HSS" and
"EEH". negative interactions between herbivore (more
strictly. folivores). and granivores could occur. With
increased productivity following high rainfall episodes.
predator exclusions should release herbivores (i.e.. degus). leading to overgrazing. and depression of seed
densities (Slobodkin et al. 1967) which would negatively
influence granivores (Oksanen et al. 1981. Oksanen and
Ericson 1987. Oksanen 1992). However. strongest
"competitor" effects between 0 . clegus and 0 . longicuudatus were present only during the El Nifio, and there
were few significant negative effects of degus on plant
cover or seed densities through 1994 (Gutierrez et al.
1997). Therefore, there may have been direct interference involving behavior rather than indirect competition through resource depletion.
Competitive interactions were more likely between
the two larger rodents, 0. degus and A. hennetti, which
have similar diets and habitats in Fray Jorge (Meserve
1981b, Meserve et al. 1983). Consumption of degus by
primarily nocturnal owls such as B. rlirginianus as well
as diurnal activity by A . bennetti refuted activity-time
separation (Rosenmann et al. 1981). Such effects should
have been greatest during the El Niiio period and
post-El Nifio when degu numbers were highest or declining (Fig. 1). There may have been a carry-over
effect of degu exclusions during the post-El Niiio resulting in greater numbers of A . hennetti then. A second
effect may have resulted from shared predators. Predators depressing numbers of degus on predator-access
grids may have switched to A. hennetti as the former
became relatively less abundant (e.g., Fig. 3). Thus. the
presence of alternative prey (degus) on degu-open grids
had a negative impact on A. hennetti. When degus were
absent, A . bennrtti became m'ore numerous during the
El Niiio and post-El Niiio on degu- as well as predatorexclusion plots. This may represent "apparent competition" (sensu Holt 1977).
Previous analyses suggested some negative effects of
0. degus on P. daric'ini and A. o1icaceu.r based on
marginally nonsignificant to significant time x competition interactions and higher numbers in degu exclusion
grids (Meserve et al. 1996). In addition, survivorship of
A. olicuce~tswas significantly greater in - D - P vs
+ D - P grids (Meserve et al. 1996). Finally, we documented negative effects of 0. degus on foraging behavior and home ranges of P. danvini and/or A. olicaceus
(P. L. Meserve and J. A. Yunger. unpubl. data). Similar
to predation. competition may exert effects that are
manifested not by numerical changes, but rather,
changes in behavior and survivorship.
While our evidence supports some biotic interactions,
exclusion of predators did not accelerate increases or
delay declines in affected species due to abiotic factors.
Therefore. while predation can be important in this
system for some species. it does not exert a controlling
effect on prey numbers nor change their demography.
Predator exclusions do not advance the timing of increases associated with El Niiio events nor prevent
declines afterwards. The magnitude of numerical effects
is particularly small on P. clur11.ini and A. berinetti
despite their high utilization in predator diets. This
effect varies temporally because mobile vertebrate
predators with strong numerical responses to prey populations focus on the thorn scrub (e.g.. Fulk 1976,
Meserve et al. 1987. Jaksic et al. 1992. 1997, Silva et al.
1995, Salvatori et al. In press).
Other species such as A. olit.aceus, A. longipilis, and
T. elegans showed little effect o f biotic interactions
and appear more sensitive to "bottom-up" factors related to rainfall. This argues against a single factor
explanation in which one interaction such as predation
acts to control small mammal prey numbers and assemblage structure. Studies showing a primary role for
predation (e.g., Goszcynski 1977, Erlinge et al. 1983.
Henttonen 1985, Henttonen et al. 1987, Desy and Batzli 1989. Hanski et al. 1991) have involved specialist
predators and or small mammal assemblages with a
single dominant prey species. Here, generalist predators were present (Jaksic et al. 1993, 1997) and prey
species had heterogeneous, decoupled population dynamics.
W e suggest that a key aspect crucial to understanding control in this system is the spatial and temporal
dynamics o f small mammal assemblage. The high spatiotemporal variability o f small mammals in other central and north-central Chilean scrub communities (e.g.,
Iriarte et al. 1989, Jaksic et al. 1992, Jimenez et al.
1992) has been interpreted as evidence for true metapopulation structure (Lima et al. 1996, Torres-Contreras et al. 1997) with independent extinction and
colonization events (sensu Hanski and Gilpin 1991,
Hansson 1991, Harrison 1991, Hanski 1994. Rosenzweig and Clark 1994). Whereas we initially viewed
the assemblage as persistent (Meserve 1981a. Meserve
and Le Boulenge 1987), here we found that some
species such as P. darltini, T. elegans, and 0. degus,
and A. olicuceus persist in the thorn scrub community.
and others such as A. longipilis and 0. longicaudatzis
disappear for varying periods. W e term the first group
"core species" (sensu Hanski 1982): A. oli~aceusmay
be a "quasi-core species" due to low numbers during
prolonged droughts. The second group ("opportunistic
species") are absent for varying perlods o f time from
the thorn scrub. Surveys o f nearby adjacent habitats in
Fray Jorge since 1996 showed that "opportunistic species" maintained breeding populations in other areas
including ridge-top fog forests ( A . longipilis), and
"aguadas" or mesic habitat in or near the valley floor
( A . longipilis, 0. longicaudatus; unpubl. data). Whereas
0. longicaudatus populations in the thorn scrub consisted o f older. non-breeding individuals conforming to
a classic source-sink model (sensu Pulliam 1988, Dias
1996), A. longipilis reproduced in the thorn scrub and
persisted for several years.
In addition to these spatial dynamics. small mammals in the thorn scrub showed temporal differences in
their responses to El Nifio events (Meserve et al. 1995,
this study), Species such as A , oliz.aceus and P,
responded most rapidly within a few months o f the
beginning o f winter rains and herbaceous plant
growth. Others such as A. long~li/is,0 . degus, and A ,
hennetti had time lags rangin&
One
two years
after high rainfall events with peaks in their numbers
well after those in primary productivity resulting in
asynchrony between their dynamics and those o f their
resources. Whereas "opportunistic species" show little
evidence for the role o f biotic factors in the thorn
scrub habitat and appear more strongly affected by
abiotic events tied to El Nifio events, "core species"
(except for T. elegans) had stronger effects o f biotic
interactions, particularly predation. However, biotic
interactions did not alter strong responses by both
"core" and "opportunistic" species to overriding abiotic factors.
Overall. our results present a mixed view as to the
evidence for "top-down" vs "bottom-up" control in
this community. Contrary to " H S S " , exclusion o f
predators while releasing herbivores such as 0. degus
did not result in many negative changes in the vegetation (Gutierrez et al. 1997). Contrary to "bottom-up"
theories (White 1978. Hunter and Price 1992), predator exclusions did have effects on some herbivorous
species. While predation effects during higher productivity periods (during and following El Nifio's), and
lack o f them during low productivity periods would be
consistent with "EEH", the heterogeneous timing o f
such effects among affected species (i.e.. 0. degus:
pre-El Nifio + El Niiio; P. darwini. A. bennetti: pre-El
Nifio + post-El Niiio) are inconsistent with a universal
productivity threshold for all species. Additional explanations for this are energetic and spatial subsidies
which influence predicted outcomes o f "top-down'' vs
"bottom-up" theories (Polis and Strong 1996). Here,
some vertebrate predators and small mammals are energetically subsidized due to omnivory (i.e.. foxes:
some small mammals such as A. olicoceus), and or
spatially subsidized with movements to from more
productive habitats (i.e., A. longipilis and 0. longicaudatus: raptors during low prey population levels).
These heterogeneous and asynchronous changes in the
spatial and temporal structure o f the small mammals
contribute to the failure o f this system to conform to
predictions o f various trophic-level models o f ecosystem control largely predicated on uniform responses
by major components.
Acknoi+.lrdgemrnts - We thank L. Oksanen for valuable comments and suggestions made on early versions of the
manuscript. In addition to the many people who have served
in the project as technicians or assistants and were previously
acknowledged as co-authors in Meserve et al. (1995). we thank
Andrea Campanella. Meredith Gooding. Alvaro Levican, Valeria Salvatori, Gaia Vaglio-Laurin, Victor Valverde, and Hernan Vasquez as well as Earthwatch volunteers in 1993-1994
for their help. We are grateful to the Corporacibn Nacional
Forestal. IV Region, and in oarticular to Marcos Cordero.
Victor Lagos. G l d o Canto. and Juan Cerda for permitting
the realization of this project in Parque Nacional Fray Jorge.
We also appreciate the cooperation of park personnel there.
S u p ~ o r for
t this proiect has come from the Graduate School.
~ d r i h e r n1llinois'~niversity. the U.S. National Science Foundation (BSR88-06639, DEB90-20047, DEB^^-18565. and
DEB96-15499), and the Fondo Nacional de Investigacibn
Cientifica y Tecnolbgica (FONDECYT 90-0930, 193-1150. and
197-0576). Chile.
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