Ecology, 95(6), 2014, pp. 1451-1457
© 2014 by the Ecological Society o f Am erica
E x p erim en tin g w ith eco sy stem in te ra c tio n n e tw o rk s in search
o f th re sh o ld p o ten tials in re a l-w o rld m a rin e ecosystem s
S im o n F . T h r u s h , 1’2’9 J u d i
E. H e w i t t , 1 S a m a n t h a P a r k e s , 1 A n d r e w M . L o h r e r , 1 C o n r a d P i l d i t c h , 3
S a r a h A . W o o d in ,4 D a v id S. W e t h e y ,4 M a r i a c h i a r a C h i a n t o r e ,5 V a l e n t i n a A s n a g h i,5 S ilv ia D e J u a n ,1
C a s p e r K r a a n , 1 I v a n R o d i l , 1 C a n d i d a S a v a g e , 6’8 a n d C a r l V a n C o l e n 7
Abstract. T hresholds p ro fo u n d ly affect o u r u n d erstan d in g a n d m an ag em en t o f ecosystem
dynam ics, b u t we have yet to develop practical techniques to assess th e risk th a t th resholds will
be crossed. C om bining ecological know ledge o f critical system interdependencies w ith a largescale experim ent, we tested fo r b reak s in the ecosystem in teractio n netw o rk to identify
th resh o ld p o ten tial in real-w orld ecosystem dynam ics. O u r experim ent w ith the bivalves
M acom ona liliana a n d A ustrovenus stutchburyi o n m arin e sandflats in N ew Z ealan d
d em o n strated th a t reductions in incident sunlight ch anged the in teractio n n etw o rk betw een
sedim ent biogeochem ical fluxes, p roductivity, a n d m acro fau n a. By d em o n stratin g loss of
positive feedbacks a n d changes in the arch itectu re o f the n etw ork, we provide m echanistic
evidence th a t stressors lead to b reak p o in ts in dynam ics, w hich th eo ry predicts predispose a
system to a critical tran sitio n .
Key words: Austrovenus stutchburyi; bifurcations; bivalves; break points; ecosystem dynamics;
M acom ona liliana; M anukau Harbour, New Zealand; marine sandflats; thresholds; turbidity.
I n t r o d u c t io n
M an y changes in ecological system s are a b ru p t,
pro fo u n d ly lim iting o u r u n d erstan d in g o f ecosystem
dynam ics, an d o u r ability to predict changes a n d cope
w ith the consequences (C arp en ter et al. 2001, Scheffer et
al. 2001). C oncern a b o u t crossing regional- a n d globalscale thresholds underscores the need to b etter define the
risk o f tip p in g an ecosystem in to ecologically a n d
socioeconom ically u n fav o ra b le states (B ro o k et al.
2013). T heories o f how critical tra n sitio n s lead to
th resh o ld change in ecological systems have progressed
rapidly, b u t em pirical su p p o rt is p atch y a n d often
focused o n specific system s, restricting generality (Kéfi
et al. 2013).
A n um ber o f techniques have been developed to
identify the statistical pro p erties o f tim e series or spatial
p attern s th a t precede th resholds (D ak o s et al. 2012,
Scheffer et al. 2012). These techniques represent a valid
w ay o f ran k in g different systems in term s o f their
M anuscript received 9 October 2013; revised 6 January 2014;
accepted 27 February 2014. Corresponding Editor: P. T.
Raimondi.
9 Present address: Institute o f M arine Science. U niversity
o f A uckland. P rivate Bag 92019. A u ck lan d 1142 New
Zealand. E-mail: sim on.thrush(® auckland.ac,nz
p red isp o sitio n to ap p ro ach in g a n d crossing thresholds,
b u t fo r real-w orld ecosystem s, this requires significant
investm ent in high-frequency m o n ito rin g th a t is gener­
ally u n com m o n (H ew itt a n d T h ru sh 2010, L indegren et
al. 2012). C onsequently, alternative a n d com plem entary
a p p ro ach es are needed to in form decisions a b o u t the
risk o f upcom ing tran sitio n s in ecosystem s a n d change
in ecosystem fun ctio n ality an d value.
T he only w ay to conclusively detect a th resh o ld is to
cross it (C arp en ter et al. 2001). Such a shift m ay result
fro m excessive en v ironm ental forcing, the fu nctional
extinction or invasion o f species, b u t m ay also occur well
below these limits due to changes in the arch itectu re o f
in teractio n netw orks th a t connect the biological, chem ­
ical, a n d physical com ponents in the ecosystem (Scheffer
et al. 2001). The loss o f positive feedbacks is p articularly
im p o rta n t in shifting the system into a fu ndam entally
different state (Scheffer et al. 2012). Such shifts in the
arch itectu re o f ecosystem in teractio n netw orks have
b een detected along en v ironm ental gradients, suggesting
the p o ten tial fo r critical tran sitio n s (T h ru sh et al. 2012).
W hole-lake experim ental m an ip u latio n s have provided
em p irical evidence o f th e im p o rta n c e o f positive
feedbacks a n d regim e shifts (C arp en ter 2003). H ow ever,
questions rem ain as to w hether we can experim entally
m an ip u late a n open an d dynam ic m arin e system to
1451
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1National Institute o f Water and Atmospheric Research, P.O. B ox 11-115, Hillcrest, Hamilton 3251 New Zealand
~Institute o f Marine Science, University o f Auckland, Private Bag 92019, Auckland 1142 New Zealand
3Department o f Biological Sciences, University o f Waikato, Hamilton 3216 New Zealand
4Department o f Biological Sciences, University o f South Carolina, 715 Sumter Street, Columbia, South Carolina 29208 USA
3Universitd degii Studi di Genova (D iS T A V ), Corso Europa 26, Genova 16132 Italy
6Department o f Marine Science, University o f Otago , P.O. B ox 56, Dunedin 9054 New Zealand
1Marine Biology Section, Biology Department, Ghent University, Krijgslaan 281-S8, Ghent 9000 Belgium
8Marine Research Institute, University o f Cape Town, Private Bag, Rondebosch, South Africa
1452
SIM ON F. T H R U SH ET AL.
Nutrients
Organic
content
Chlorophyll a
Macomona
Mud '
content
Austrovenus,
13
10
\
Coarse
sediment
F i g . 1. Conceptual diagram of the potential interaction
netw ork linking infaunal bivalves (here m arine species M aco­
mona liliana and Austrovenus stutchburyi in New Zealand) to
benthic chlorophyll a and sediment characteristics. (1) Grazing
by deposit-feeding M acomona affects m icrophytobenthos
(MPB, represented as chlorophyll a), and MPB has a positive
relationship with Macomona density. (2) Sediment organic
content increases food resources for Macomona. (3) MPB are
highly productive and exploit nutrients rem ineralized in
sediments. (4) Macomona affect pore water nutrient concentra­
tions directly and (2, 5) indirectly. (6) Austrovenus has a positive
effect on MPB. (7) Large Macomona and small Austrovenus
interact negatively. (8, 9) Sediment m ud content negatively
affects density of both bivalve species; high densities of both
species can increase fine-sediment erosion. (10) In coarse
sediments, Austrovenus density increases. (11) MPB and m ud
content have a positive relationship, (8, 9) m ediated by resident
m acrofauna. (12) M ud and sediment organic content are tightly
correlated and (13) coarse sediments influence sediment organic
content by increasing permeability and decay. (14) Degrading
MPB also contributes to sediment organic m atter, which (5) is
positively correlated with nutrient concentration in pore water
through microbial degradation. See M ethods for further details
and references.
dem onstrate changes in in teractio n netw orks a n d the
loss o f positive feedbacks. W e provide a p a th to address
critical tra n sitio n s th a t facilitate a fo rm a l linkage
betw een em pirical a n d th eoretical study o f ecosystem
dynam ics. A s pred icted by th eo retical studies, o u r
experim ent dem on strates th a t stress-induced changes in
ecosystem interactio n netw orks can occur in real-w orld
ecosystems, and this allows us to determ ine w hether or
n o t a specific ecosystem is predisposed to u ndergo
tran sitio n s. Such em pirical d e m o n stra tio n helps to
g ro u n d theory and provide real-w orld advice to su p p o rt
m anagers, policy m akers, an d society a b o u t the limits to
resilience o f ecosystem s u n d er change.
There is a long h istory o f ecological ex p erim entation
in m arine systems, w ith early recognition o f the role o f
interactions am ong species a n d distu rb an ce influencing
com m unity dynam ics (D ay to n 1971, W o o d in 1978).
N ew analytical techniques allow us to assess the strength
o f b o th direct and indirect effects, define the architecture
o f interaction netw orks, an d assess its validity relative to
em pirical d a ta (G race et al. 2012). S tru ctu red eq u atio n
Ecology, Vol. 95, No. 6
m odels (SE M s) allow us to in te g rate cau sal an d
ex p lo rato ry techniques, beginning w ith the developm ent
o f a conceptual m odel su p p o rted by em pirical evidence.
O ur conceptual m odel (Fig. 1) is focused on interactions
am ong prim ary producers, tw o sediment-dwelling bivalves
(the deposit feeder M acom ona liliana an d the suspension
feeder Austrovenus stutchburyi), sedim ent type, an d pore
w ater nutrien t an d organic m atter pools, justified by
empirical research an d know ledge o f ecosystem function­
ing. The p otential for interaction betw een these variables
an d analogous species is typical o f shallow, non-eutrophic,
coastal an d estuarine sandflat systems. This interaction
netw ork has some o f the same elements as those previously
used to look for thresholds across environm ental gradients
(T hrush et al. 2012). The conceptual m odel represents an
ecosystem in terac tio n n etw o rk th a t su p p o rts coastal
ecosystem services associated w ith h a b ita t stability,
nu trien t recycling, an d productivity (B arbier et al. 2011).
In this paper we test for changes in the architecture o f the
ecosystem interaction netw orks (Fig. 1) associated w ith
decreased light levels, an im p o rta n t consequence o f
increased turbidity in coastal ecosystems. W e developed
SEM s based on experim ental d ata derived from either
shaded or unshaded experim ental plots. Changes in land
use often elevate terrestrial sedim ent an d n u trien t loading
in m an y estuarine a n d coastal ecosystem s. E levated
turbidity is generally recognized because o f its negative
effects on seagrass (D u arte 2002), w hereas effects on
m icrophytobenthos are often overlooked despite their
central role in p rim ary productivity, nutrien t interception,
an d basal food resource provisioning for m any benthic
invertebrates.
M eth o d s
SE M starts w ith th e d efinition o f th e p o te n tia l
in teractio n n etw o rk (num bered effects discussed here
refer to num bers in the Fig. 1 netw ork). Specifically, (1)
there is a direct negative effect o f the large depositfeeding M acom ona on m icro p h y to b en th o s (M PB; re p ­
resented as chlorophyll a) due to grazing (Lelieveld et al.
2003). M PB are an im p o rta n t fo o d source fo r M a co ­
m ona, b u t there is also a positive relationship betw een
chlorophyll a biom ass a n d M acom ona density (T h ru sh
et al. 2006). Sim ilarly, (2) sedim ent organic co n ten t
increases the fo o d resources for M acom ona (by analogy
to the functionally sim ilar species M acom a balthica
[Peterson a n d Skilleter 1994]). (3) M PB are highly
p ro d u c tiv e (C a h o o n 1999) a n d rely o n n u trie n ts
rem ineralizing in sedim ents to sustain th a t p ro d u ctio n
(L o h rer et al. 2004). M acom ona affects p o re w ater
n u trie n t co n cen tratio n s directly (4) an d indirectly (2 an d
5) th ro u g h influencing organic m a tte r pools via grazing
an d behaviorally induced pressure gradients in p erm e­
able sedim ents (V o lkenborn et al. 2012, W oo din et al.
2012). (6) Austrovenus has a positive effect on ch lo ro ­
phyll a (T h ru sh et al. 2006), alth o u g h this effect is
density depen d en t (Sandw ell et al. 2009, L o h rer et al.
2011). (7) N egative in teractio n s betw een large M acom o-
T H R E SH O LD PO TEN TIA L IN M A R IN E ECOSYSTEM S
lia an d sm all Austrovenus have specifically identified
(T h ru sh et al. 1996). (8 an d 9) D ensities o f b o th bivalve
species are negatively im pacted by m u d (T h ru sh et al.
2003, 2004), b u t high densities o f b o th species can
increase the erosion o f fine sedim ents by b io tu rb a tio n
(T h ru sh et al. 1996, Jones et al. 2011). (10) In coarse
sedim ents, A ustrovenus density increases (T h ru sh et al.
2008). (11) A positive relationship betw een benthic
chlorophyll a a n d sedim ent m uddiness exists (Y an de
K oppei et al. 2001), due to fine-sedim ent binding by
M B P, a relationship (8 a n d 9) m ed iated by resident
m acro fau n a (Y an C olen et al. 2013). (12) M u d an d
sedim ent organic co n ten t are tightly co rrelated (Sloth et
al. 1995) a n d (13) coarse sedim ents influence sedim ent
organic content by increasing perm eability a n d acceler­
ating decay rates (H uettel a n d R usch 2000). D egrading
chlorophyll a (14) also contrib u tes to the p o o l o f organic
m a tte r in the sedim ent (E hrenhauss et al. 2004), a n d (5)
the concen tratio n o f pore w ater n u trien ts is positively
correlated w ith th e sedim ent organic co n ten t th ro u g h
m icrobial d eg ra d a tio n processes (S loth et al. 1995,
G rabow ski et al. 2011).
T he experim ent w as co n d u cte d at W iro a Island,
M an u k au H arb o u r, N ew Z ealand (37°01.3' S, 174°49.2'
E; see Plate 1). The intertidal sandflat is ~ 1 .8 km wide
an d has a shallow gradient o f 0.097° (T hrush et al. 1997).
T he m acro fau n a l com m unity o f the W iro a Islan d
sandflats is dom in ated b o th num erically a n d in term s of
biom ass by the tellinid M acom ona liliana ( ~ 100/m2 for
individuals w ith shell length > 2 0 m m ), a n d the venerid
Austrovenus stutchburyi ( ~ 3 2 /n r for individuals w ith
shell length > 10 m m ). T o investigate differences in the
architecture o f the ecosystem interaction netw ork, we
experim entally m an ip u lated nutrien t concentrations, M a ­
comona densities, a n d light. The experim ent was estab­
lished on 25-29 O ctober 2011 in seven blocks th at
encom passed ab o u t 800 X 350 m o f sandflat. E xperim en­
tal plots ( 2 X 2 m ) were situated a b o u t 3 m ap a rt in three
row s to encom pass an area o f a b o u t 56 m alongshore an d
14 m dow nshore. The experim ent consisted o f three
density treatm en ts o f M acom ona (200, 50, an d 0
individuals/m 2 for individuals w ith shell length > 20
m m ) crossed w ith three light treatm ents (shade, shade
control, a n d open) crossed w ith three nutrien t addition
treatm en ts (high, m edium , none) a n d one am bient
sedim ent treatm ent. This resulted in 28 experim ental
treatm ents, replicated once per block.
T he central 1 in 2 in each 4-m 2 plo t, excluding one
treatm en t o f am bient sedim ent, w as excavated to 18 cm
d ep th a n d the sedim ent sieved on 10-m m m esh to extract
shell h ash an d large m acro fau n a. Sedim ents were then
retu rn ed to the excavated plots an d M acom ona (> 2 0
m m shell length) were spread evenly across the 1 in 2
achieve treatm en t densities.
Shade cloth designed to cut ~ 7 0 -8 0 % o f the incident
light w as su p p o rted o n a 4 - n r m etal grid (m esh size 150
X 150 m m ) suspended 15-20 cm above th e sedim ent
surface. Shade c o n tro ls w ere th e m etal g rid only
1453
covering the plots. Shading o f plots w as used to m im ic
changes in light levels due to elevated susp en d ed
sedim ent co n cen tratio n s, SSC (Billerbeck et al. 2007).
D irect field-based m an ip u latio n o f SSC is very difficult
in the m edium to long term . A lth o u g h SSC has m ultiple
effects o n the ben th o s (T h ru sh et al. 2004), we focused
o n effects m ed iated th ro u g h the M PB . Benthic ch lo ro ­
phyll a is a m easure o f M PB stan d in g stock, n o t
productivity. T his is im p o rta n t in the in te rp re ta tio n o f
o u r ex p erim en t due to th e p o te n tia l fo r b e d lo a d
tra n s p o rt o f M P B u n d er sh ad ed p lo ts, p o ten tially
w eakening treatm en t effects.
N u trien t ad d itio n consisted o f a d d in g fo u r (high), one
(m edium ), o r zero 10 cm long sections o f dialysis tubing
filled w ith 15 g (± 0 .1 g) o f a g ran u lar slow-release
fertilizer (nu trien t ratios: 18.9 N , 2.1 P, 0.0 K , 4.1 S, 3.0
M g, 7.2 Ca). O u r n u trien t a d d itio n treatm en ts were
expected to have a direct stim u lato ry effect o n M PB ,
because N ew Z ealan d sandflat studies show th a t M PB
resp o n d to n u trien t released from the sedim ent as a
result o f b io tu rb a tio n (R odil et al. 2011).
B efore d estru ctiv e sam p lin g a t th e en d o f the
experim ent (ab o u t +100 days, 7-10 F eb ru ary 2012),
p o re w ater n u trien ts sam ples were collected from each
p lo t using reservoirs sam pling the perm eable sedim ents 5
cm below the sed im en t-w a ter interface. P ore w ater w as
pressure-filtered th ro u g h a 2.5-cm W h a tm a n G F /C glass
fiber filter in a Swinnex filter h o ld er (E D M illipore,
Billerica, M assachusetts, U SA ) a n d stored o n crushed
ice in the d a rk fo r tra n sp o rt to the lab o rato ry , w here
they were frozen to —20°C pending analysis. A nalysis for
dissolved inorganic n u trien ts follow ed sta n d a rd m eth o d s
fo r seaw ater using a n A storia-Pacific 300 series segm ented-flow au to an a ly zer (A storia-Pacific, C lackam as,
O regon, U SA ) w ith d etection lim its o f <0.1 pm ol/L for
N a n d P. T hree cores (2.3 cm diam eter, 2 cm deep) were
collected fro m each plo t a n d w ere p o o led fo r chlorophyll
a , sedim ent particle size, a n d organic co n ten t analyses.
T he rem aining sedim ent w ithin the central 1 m 2 w as
excavated to a d ep th o f a b o u t 15 cm a n d sieved on 10m m m esh to extract large m acro fau n a, w hich were then
identified a n d sized.
Sedim ent fo r chlorophyll analysis w as freeze-dried
a n d hom ogenized. A sm all q u a n tity o f sedim ent (—0.1 g)
w as soaked in 10 m L o f M g C 0 3-buffered acetone (90%)
fo r ~ 2 0 h. Sam ples w ere shaken after 12 h an d again
p rio r to centrifugation. Sam ples w ere centrifuged fo r 10
m in a t 3300 rp m before fluorom etric analysis (T u rn er
10-A U , T u rn e r D esigns, Sunnyvale, C alifornia, U SA ).
A n acidification step (0.15 m L 0.1N H C L ) w as used to
sep arate p h aeo p h y tin from p h o to sy n th etic pigm ents
(A ra r a n d C ollins 1997). T o tal organic m a tte r con ten t
(as a percentage) w as d eterm ined th ro u g h loss on
ignition from hom ogenized dried sedim ents (105°C for
24 h o r un til stable m ass), after com b u stio n fo r 5.5 h at
550°C (D ean 1974). Sedim ents fo r particle size analysis
w ere digested in 10%) h y drogen peroxide to rem ove
organic m atter, until b ubbling ceased before using the
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June 2014
1454
SIM ON F. T H R U SH ET AL.
Ecology. Vol. 95. No. 6
P l a t e 1.
Outplanting Macomona in one of the experimental plots on the sandflat (W iroa Island. New Zealand). Photo credit:
Rachel J. Harris.
sta n d ard operating p rocedure fo r m arine sedim ents o n a
M alvern m astersizer-S (300 F R lens; M alv ern In s tru ­
m ents, M alvern, U K ) to determ ine grain size fractions in
the range o f 0.05-2000 pm.
SEM s were developed using M -P lus softw are (M u th én an d M u th én 2007), based o n Fig. 1, to co n tra st the
netw orks a p p aren t in the shaded an d u n sh ad ed exper­
im ental treatm ents. W e developed best-fit m odels for
shaded a n d unsh ad ed treatm en ts a n d co m p ared these
w ith the results from applying the best shaded n etw ork
to the unsh ad ed d a ta a n d vice versa, in o rd er to ensure
th a t there were real differences in the netw orks. D a ta
tra n sfo rm a tio n s (loge) to im p ro v e th e lin earity o f
responses, or n orm ality o f errors, w ere utilized for
bivalve abundances, coarse sand, a n d m ud. The initial
SE M (Fig. 1) w as exam ined fo r respecification by
rem oval o f direct p athw ays based o n p a ram eter tests
o f significance, while m ain tain in g nonsignificance tests
fo r goodness o f fit (x2) a n d the ro o t m ean square erro r
o f ap p ro x im atio n , increasing values o f the co m parative
fit index (above 0.95) (Vile et al. 2006) a n d decreasing
A k aik e’s in fo rm atio n criterio n (see A ppendix). The
sensitivity o f the m odel to new direct p athw ays w as
also investigated, w ith the decision on w hether o r n o t to
include new links being based o n p ara m e te r significance
tests an d n o decreases in goodness o f fit (G race et al.
2 012).
R esu lts
C onsistent w ith using SE M as a to o l to integrate
causal a n d ex p lo rato ry techniques (G race et al. 2012),
we have n o t focused on the m o re trad itio n al analyses o f
the experim ental d ata. Prelim inary analysis d id n o t
ind icate any experim ental a rtefacts asso ciated w ith
sh ad in g (see A p p en d ix ). T re a tm e n t differences in
M acom ona density were m ain tain ed in the experim ent,
a lth o u g h slightly higher densities in shaded plots were
a p p a re n t, while Austrovenus decreased. L ow er pore
w ater N O x co n cen tratio n s w ere fo u n d in higher M a co ­
mona density a n d zero n u trien t a d d itio n treatm ents.
P o re w ater dissolved reactive p h o sp h o ru s co n cen tra­
tio n s w ere significantly a n d n egatively re la te d to
M acom ona density, b u t n o t n u trie n t a d d itio n . N o
significant differences in benthic chlorophyll a concen­
tra tio n o r p o re w ater am m onia co n cen tratio n s were
detected. A lth o u g h m ean benthic chlorophyll a concen­
tra tio n s in the shaded plots were low, high variability
lim ited the d etec tio n o f significant differences (see
A ppendix).
S h ad in g d rastica lly ch an g ed th e n a tu re o f the
in teractio n netw o rk (Fig. 2). In the u n sh ad ed tre a t­
m ents, there w ere a to ta l o f 13 interactions; alth o u g h
three w ere w eak (P > 0.15 fo r estim ates), they were
req u ired fo r m odel stability. A positive feedback loop
w as identified betw een Austrovenus, benthic chlorophyll
June 2014
T H R E SH O LD PO TEN TIA L IN M A R IN E ECOSYSTEM S
Unshaded
Shaded
Nutrients
0.02
H
Nutrients
Chlorophyll a
0.24
Chlorophyll a
0.24 .,
Organic
^ c o n te n t 0.19
Organic
content 0.07
Macomona
0.07 ,
Macomona
Austrovenus
0.30 ▼
1455
Mud
0.30
Coarse
sediment
Austrovenus
0.18
' A
Mud
0.10
Coarse ■'
sediment
a, a n d m ud. A positive coarse sed im en t-o rg an ic m a tte r
link fed into this positive feedback loop. A n o th e r w eak
positive feedback loop involving M acom ona releasing
n u trien ts to su p p o rt chlorophyll standing stock fed into
the stronger feedback loop.
In co n trast, in the shaded plots, only seven connec­
tions w ere m ade a n d there w ere n o positive feedbacks.
T he positive feedback betw een Austrovenus, benthic
chlorophyll a, an d m u d w as b ro k en a t the link betw een
benthic chlorophyll a a n d m u d , w hich w as now negative,
an d the positive effect o f M acom ona o n A ustrovenus was
also lost. A dditionally, the negative effect o f M acom ona
o n benthic chlorophyll a w as now significant a n d the
positive effect o f chlorophyll a o n M acom ona h a d been
lost. A lth o u g h b o th bivalves play a central role in the
in teractio n n etw o rk u n d er am b ien t light, w hen the
sedim ent is shaded, th eir role, a n d in p artic u la r the
positive feedbacks, are n o t ap p aren t. U n d e r shaded
conditions, we see m ostly simple u n idirectional relatio n ­
ships betw een biological a n d physical variables, w ith no
role fo r n u trien t additions.
D is c u s s io n
O u r em pirical evidence o f a b reak p o in t is consistent
w ith theoretical predictions o f a system predisposed to a
th resh o ld shift, w hich w o u ld occur in response to
changes in sedim ent loading a n d eu tro p h icatio n . These
stresso r-in d u ced changes im ply im p o rta n t shifts in
ecosystem interactions th a t determ ine organic m a tte r
deg rad atio n , n u trien t recycling, an d pro d u ctiv ity th a t
drive the functional capacity o f co astal soft sediments.
T he reconfiguration o f the in teractio n n etw ork, as a
result o f shading, occurred in a b o u t 100 days an d
resulted in the loss o f positive feedbacks b o th directly by
linking large M acom ona w ith M P B a n d indirectly
m ed iated th ro u g h large Austrovenus (Fig. 2). In a d d i­
tio n , the n u trien t ad d itio n s m ed iated the in teractio n
betw een M acom ona a n d M P B only in th e u n sh ad ed
sedim ents. A lth o u g h m ean M PB w as low er in shaded
tre a tm e n ts, h ig h v ariab ility p reclu d ed d etec tin g a
significant difference. A n im p o rta n t fa c to r on this
sandflat is the b ed lo ad tra n sp o rt o f surficial sedim ents
a n d associated M P B (T u rn e r et al. 1997). T his process
p rovides a m echanism to resupply M PB to shaded
sedim ents a n d a d d variability to o u r d ata . N evertheless,
o u r experim ent w as able to detect significant changes in
the ecosystem in teractio n netw ork. A t the scale o f o u r
experim ent, the m echanism s o f change induced by large
M acom ona are behaviors (b io tu rb atio n , feeding, gili
cleaning, gut voiding) th a t affect pore w ater oxygen
co n cen tratio n s a n d n u trien t cycling (Y o lk en b o rn et al.
2012). M ed iatio n o f the effects o f n u trien t a d d itio n s by
large bivalves only in u n sh ad ed plots highlights the
p o ten tial fo r cum ulative effects associated w ith in ­
creased tu rb id ity an d eutrop h icatio n .
SEM s revealed th a t shading the sedim ent decoupled
the ecosystem role o f M acom ona in sedim ent b iogeo­
chem istry. The range o f d a ta encom passed in m odel
b uilding is im p o rta n t in generalizing the SEM . A lthough
th e differences in en v iro n m en tal cond itio n s en co m ­
p assed in this experim ent w ere subtle, the in teractio n
n etw o rk m odels developed fro m this experim ent were
sim ilar to those previously developed from broadscale
surveys o f large b io tu rb a tin g fau n a, sedim ent grain size,
o rg an ic ch ara c teristics, a n d b en th ic c h lo ro p h y ll a
(T h ru sh et al. 2012). T he previous analysis revealed
shifts in n etw o rk arch itectu re across a benthic ch lo ro ­
phyll a th resh o ld o f 11.6 pg/g chlorophyll a. D espite the
sm aller range o f d ata in o u r m o re recent experim ent, a
sim ilar th re sh o ld w as d etec ted, im plying th a t the
SlAOcCdiL
F ig . 2. Changes in ecosystem interaction networks associated with experimental shading, showing R 2 values for each factor.
Red arrow s indicate positive effects, black lines indicate negative. Solid lines denote param eter estimates with P < 0.05; dotted lines
with P values 0 .0 5 -0 .1 5 ; dashed lines with P > 0 .1 5 . but the relationship needs to be retained in the model for stability. Line
thickness increases with the size of the param eter estimate, standardized by the relevant range standardization procedure (Grace et
al. 2012); actual values are presented in the Appendix.
1456
SIM ON F. T H R U SH ET AL.
netw orks are reasonably stable a n d consistent. F u n d a ­
m ental shifts associated w ith a loss o f positive feedbacks
an d restrictions in the im p o rtan ce o f indirect effects were
ap p a re n t in b o th this ex p erim en tal stu d y a n d the
previous broadscale analysis. P roviding em pirical in fo r­
m atio n to define how a set o f ecosystem com ponents are
connected in an in teractio n n etw o rk helps to elucidate
ecosystem fu nctio n . M o reo v er, if specific types o f
co n n ectio n s a re p resen t, b u t can be c h an g ed by
particu lar stressors, this provides a useful m eans for
predicting the risk o f critical tra n sitio n related to a
specific type an d m agnitudes o f stress. It also allows
insight into ecosystem fu n ctio n after the tran sitio n .
A lth o u g h there is often a gap betw een th eo ry an d
practice, we have been able to experim entally shift the
architecture o f an in teractio n netw ork, p roviding m ore
im p etu s fo r scientists a n d m an a g e rs to use these
indicators o f critical tran sitio n s. O u r results show th a t
w ell-designed an d scaled m anip u lativ e field experim ents
can contribute to identifying w arnings o f increased risk
fo r upco m in g ecosystem tra n sitio n s by testin g fo r
changes in in teractio n netw orks. F o r exam ple, specific
experim ents m an ip u latin g the level o f shading could be
designed an d im plem ented in different locations to
define key b reak p oints fo r resource m anagem ent. Shifts
in functional perform ance associated w ith shading m ay
n o t be g rad u al if in teractio n netw orks fu ndam entally
shift. In o u r experim ent, we see changes associated w ith
interactions th a t affect key attrib u te s o f the system
ranging from p rim ary pro d u ctiv ity a n d the stabilization
o f fine sedim ents to th e ability o f the system to recycle
key nutrients. This indicates th a t the m ain ten an ce o f
com m unity functio n plays critical roles in the resilience
o f sandflats to elevated suspended-sedim ent co n c en tra ­
tions an d eutrophicatio n .
C hange associated w ith non-p o in t-so u rce lan d use,
sedim ents, an d n u trien ts are noto rio u sly difficult to
m anage. H ow ever policies th a t generate inertia a n d are
blin d to o th er surprises are d angerous a n d ultim ately
m ay be very costly in term s o f the loss o f ecosystem
services an d associated societal values (H o ra n et al.
2011). This is w hy th e risks o f th resh o ld shifts are
im p o rtan t. If n o t pro p erly accounted for, o u r futures
m ay be m ark ed by sudden, unexpected reductions in
ecosystem functionality a n d value. I f there is a credible
risk th a t a p articu la r system can change in a n o n lin ear
w ay associated w ith subtle b u t cum ulative stress, then
m anagem ent dow n to a p redeterm ined lim it will be
highly risky. O u r a p p ro a c h o f investigating the arch i­
tecture o f ecosystem in teractio n netw orks, a n d how they
are changed by stressors, provides real-w orld em pirical
evidence to su p p o rt m an y o f the theo retical develop­
m ents in regim e shifts a n d resilience. This will allow us
to m o re tan g ib ly u n d e rs ta n d th e im p licatio n s o f
thresholds in ecosystem s th a t affect o u r daily lives.
A lth o u g h we can n o t yet predict w hen b reak p o ints in
d ynam ics w ill occur, o u r a p p ro a c h do es identify
m echanistic links a n d the key connections betw een
Ecology. Vol. 95. No. 6
ecosystem elem ents th a t will facilitate interventions.
Such interventions are im p o rta n t in averting regime
shifts, especially w here the drivers o f change are difficult
to ad ju st o r generate huge legacy effects (Biggs et
al. 2009).
A cknow ledgm ents
We thank the Auckland Council for permission to conduct the
experiment (CN37056:FN12876) and Peter Robinson (Grounds
and Wildlife H azard M anagem ent Planner for Auckland
Airport) and Aviation Security for access to the study site. We
thank Katie Cartner, Iain M acDonald. Barry Greenfield. Sarah
Hailes. Michael Townsend. Hazel Needham. Carolyn Lundquist,
and others involved with the fieldwork and laboratory analysis.
This work was funded by M BIE CO 1X1005 and N IW A under
the Coasts and Oceans Research Programme 3 (2012/13 SCI). C.
K raan was supported by the M arsden Fund. Royal Society of
New Zealand (NIW1102), and a Marie-Curie International
Outgoing Fellowship (FP7-PEOPLE-2011-IOF). C. Van Colen
acknowledges a postdoctoral fellowship provided by the Flemish
Fund for Scientific Research (FWO-1.2.380.11.N.00).
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S u p p le m e n ta l M a t e r i a l
Appendix
Description o f experimental effects and potential artifacts and base statistical tables structured equation modeling (Ecological
Archives E095-127-A1).
SlAOcCdiL
June 2014