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ARTICLE
Top-down versus bottom-up: Grazing and upwelling regime
alter patterns of primary productivity in a warm-temperate
system
Abby R. Gilson | Christopher McQuaid
Department of Zoology and Entomology,
Rhodes University, Grahamstown,
South Africa
Correspondence
Abby R. Gilson
Email: gilsona@tcd.ie
Funding information
National Research Foundation; Rhodes
University
Handling Editor: Erik E. Sotka
Abstract
Community structure is driven by the interaction of physical processes and
biological interactions that can vary across environmental gradients and the
strength of top-down control is expected to vary along gradients of primary
productivity. In coastal marine systems, upwelling drives regional resource
availability through the bottom-up effect of nutrient subsidies. This alters rates
of primary production and is expected to alter algae–herbivore interactions in
rocky intertidal habitats. Despite the potential for upwelling to alter these
interactions, the interaction of upwelling and grazing pressure is poorly under-
stood, particularly for warm-temperate systems. Using in situ herbivore exclu-
sion experiments replicated across multiple upwelling regimes, we
investigated the effects of both grazing pressure, upwelling, and their interac-
tions on the sessile invertebrate community and biomass of macroalgal com-
munities in a warm-temperate system. The sessile invertebrate cover showed
indirect effects of grazing, being consistently low where algal biomass was
high at upwelling sites and at nonupwelling sites when grazers were excluded.
The macroalgal cover was greater at upwelling sites when grazers were
excluded and there was a strong effect of succession throughout the experi-
mental period. Grazing effects were greater at upwelling sites, particularly dur-
ing winter months. There was a nonsignificant trend toward greater grazing
pressure on early than later successional stages. Our results show that the posi-
tive bottom-up effects of nutrient supply on algal production do not over-
whelm top-down control in this warm-temperate system but do have
knock-on consequences for invertebrates that compete with macroalgae for
space. We speculate that global increases in air and sea surface temperatures
in warm-temperate systems will promote top-down effects in upwelling
regions by increasing herbivore metabolic and growth rates.
Received: 13 October 2022 Revised: 21 July 2023 Accepted: 25 August 2023
DOI: 10.1002/ecy.4180
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any
medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2023 The Authors. Ecology published by Wiley Periodicals LLC on behalf of The Ecological Society of America.
Ecology. 2023;104:e4180. https://onlinelibrary.wiley.com/r/ecy 1of17
https://doi.org/10.1002/ecy.4180
KEYWORDS
algae–grazer interactions, bottom-up control, coastal marine ecosystems, ecosystem
functioning, grazer exclusion, nutrient subsidies, top-down control
INTRODUCTION
Community structure varies significantly through space
and time and particularly varies across environmental
gradients (Burkepile & Hay, 2006; Hillebrand, 2002;
Sellers et al., 2020; Worm et al., 2002). Understanding the
processes that drive trophic structure and community
composition has been the focus of ecological research for
decades (Hairston et al., 1960; Leibold et al., 1997). Early
ecological models focused on the role of resource avail-
ability (i.e., bottom-up effects), predicting that the
strength of top-down control varied along gradients of
primary productivity (Bustamante et al., 1995; Fretwell,
1987; Loreau, 2001; Menge & Menge, 2013; Navarrete
et al., 2005; Nielsen & Navarrete, 2004; Oksanen et al.,
1981). This understanding was based on studies under-
taken at local scales that focused on the role of species
interactions in shaping community structure (Witman
et al., 2015), however the predictive role of regional-scale
processes is now becoming increasingly recognized
(Coleman et al., 2006; Jenkins et al., 2005). Given current
changes in climate, predicting the dynamics of commu-
nity structure requires an approach that highlights the
importance of regional processes and resource flow
across boundaries (Hacker et al., 2019; Loreau & Holt,
2004; Menge & Menge, 2013; Sellers et al., 2020).
Resource subsidies (energy, material, organisms) can
have significant impacts on local community structure,
dynamics and functioning and are fundamental to under-
standing the connections between ecosystems across
large spatial scales (Loreau & Holt, 2004; Polis et al.,
1997). Nutrient subsidies in particular play a key role in
determining trophic structure, affecting energy transfer,
consumer dynamics and food-web stability (Barnes et al.,
2018; Larsen et al., 2016; Moore et al., 2004). Ecological
theory predicts that primary producers are resource lim-
ited, with nutrients determining the ability of herbivores
to reduce plant biomass via bottom-up control (Hairston
et al., 1960). An increase in nutrient availability, there-
fore, can drive increases in primary productivity,
resulting in increases in secondary production, greater
herbivore densities and subsequent top-down control of
primary producers (Bosman et al., 1987; Bustamante
et al., 1995; Nielsen & Navarrete, 2004; Pulgar et al.,
2013; Shurin et al., 2006).
In rocky intertidal systems, nutrient subsidies from
cold, nutrient-rich water linked to coastal upwelling
events have been shown to alter species interactions sig-
nificantly (Blanchette et al., 2009; Broitman et al., 2001;
Bustamante et al., 1995; Menge & Menge, 2013).
Although the effects of upwelling have been shown to
affect primary producers positively through increases in
productivity, growth rates, and cover, the effects on sec-
ondary production and top-down control are more com-
plex. Contrary to ecological theory, a recent
meta-analysis of studies involving the effects of coastal
upwelling on top-down control of primary producers
found that upwelling events weaken herbivore effects
and reduce top-down control in coastal systems (Sellers
et al., 2020). Such contradictions are thought to be driven
by a combination of co-occurring processes. First, nutri-
ent subsidies increase primary production and producer
growth rates and overwhelm top-down control by herbi-
vores. Second, offshore larval advection resulting from
the surface currents that drive upwelling limits consumer
recruitment in species with dispersive larvae, decoupling
larval production from recruitment (Blanchette et al.,
2006; Broitman et al., 2001; Connolly et al., 2001; Wieters
et al., 2008). In addition, it has also been suggested that
the colder temperatures associated with deep, upwelled
water may reduce herbivore metabolic rates, reducing
grazing intensity during upwelling events (Bruno et al.,
2015; Kishi et al., 2005). Upwelling, however, increases
primary production and drives greater food availability
and quality, which has been shown to support larger
individuals, suggesting that per capita grazing effects
may be greater under upwelling regimes (Nielsen &
Navarrete, 2004). Given that ocean warming is predicted
to increase rates of primary productivity and alleviate
herbivore metabolic constraints, understanding these
relationships is critical to predicting changes to food-web
structure and dynamics (O’Connor, 2009). To date,
research to disentangle the effects of grazing across
upwelling regimes has been limited and covers a narrow
geographical range, making it difficult to draw general
conclusions.
Intertidal rocky shores are patchy mosaics of commu-
nity assemblages compromising macroalgal and inverte-
brate communities at different stages of succession
(Masterson et al., 2008). Early experimental manipula-
tions highlighted the ability of intertidal grazers to con-
trol primary producer species composition through the
consumption of algal propagules, providing available
space for the colonization of sedentary invertebrates such
2of17 GILSON and MCQUAID
as mussels and barnacles (Hawkins & Hartnoll, 1983;
Jenkins et al., 2005). Enhanced nutrient supply has been
shown to drive changes in algal diversity, resulting in
enhanced growth of early successional, opportunistic spe-
cies with low levels of antigrazing properties (Kraufvelin
et al., 2002; Worm et al., 2000). An increase in palatable,
ephemeral species via bottom-up effects can alter
top-down control through increases in grazer density and
the size of grazer populations. The interactive effects of
top-down and bottom-up processes, therefore, can be
reflected in community processes such as succession
(Worm et al., 2000,2002). Life history traits, particularly
feeding mode and body size, can also significantly alter
spatial patterns, with different types and size classes of
grazers simultaneously exploiting different resources,
increasing the strength of top-down control (Burrows &
Hawkins, 1998; Díaz & McQuaid, 2011; Hawkins &
Hartnoll, 1983; McQuaid, 1996; Santini et al., 1991). In
addition, modifying factors such as physical stress and
disturbance can interact both directly and indirectly with
bottom-up and top-down processes to regulate intertidal
community structure (Hawkins & Hartnoll, 1983;
Thompson et al., 2004).
The Atlantic coast of South Africa is characterized
by the eastern boundary Benguela Current and upwell-
ing driven by southeast trade winds. In contrast, the
Indian Ocean coastline on the south and east coasts is
dominated by the Agulhas Current that brings warm
water southward from Mozambique to the edge of the
Agulhas Bank (Lutjeharms, 2006). As a result, the west
coast can be considered cold temperate, the south coast
warm temperate, and the east coast subtropical (Cole &
McQuaid, 2011; Emanuel et al., 1992;Stephensonetal.,
1937). Both topographic and wind-driven upwellings do
occur on the east and south coasts, however, with at
least one site of semipermanent upwelling on the
south coast (Goschen et al., 2015;Lutjeharms,2006).
Upwelling can also be associated with onshore/offshore
meandering of the Agulhas Current (Goschen et al.,
2015). Despite the occurrence of upwelling and large
grazer populations, only one study in South Africa has
explicitly incorporated both grazing pressure and
upwelling (Ndhlovu et al., 2021), and only a few others
have explicitly manipulated grazing or nutrient avail-
ability (Bustamante et al., 1995;Dye,1995;Maneveldt
et al., 2009).Inaddition,inlinewithecologicaltheory
and in contrast with the majority of the studies investi-
gating the effects of upwelling on top-down and
bottom-up control, these studies have identified
increased grazing pressure associated with increased
upwelling. However, these few studies quantify grazing
pressure as increased population densities and do not
explicitly test for total grazing or per capita effects on
algal productivity under contrasting upwelling regimes.
Given the predicted changes to wind-driven upwelling
events and ocean warming under future climate change
scenarios, understanding top-down and bottom-up
effects and how they interact to alter community struc-
ture and functioning is critical to predicting and under-
standing the knock-on effects of human-mediated
change.
We established an in situ manipulative experiment at
four sites along the warm-temperate southeast coast of
South Africa. These sites differed in the intensity and fre-
quency of upwelling they experienced, allowing us to test
explicitly the effects of upwelling on macroalgal produc-
tion in the presence and absence of grazers, and how these
effects change over time. The experimental design also
allowed us to investigate the effects of upwelling and graz-
ing pressure on different successional stages of macroalgal
communities and colonization by sessile invertebrates.
Four hypotheses were tested; compared with
nonupwelling sites, upwelling sites will exhibit: (1) lower
cover of sessile species in both the presence and absence of
grazers; (2) higher macroalgal production in the absence
of grazers; (3) stronger grazing effects on macroalgae par-
ticularly in winter (June–August); and (4) grazing pressure
will be greater in early successional stages at both upwell-
ing and nonupwelling sites due to the lack of physical or
chemical defenses in early colonizers.
METHODS
Upwelling
The south and east coasts of South Africa are dominated
by the Agulhas Current that is fed by the Mozambique
Current and a tributary of the East Madagascar Current.
It drives warm water poleward along the shelf edge of
southern Africa and deflects offshore as the Agulhas ret-
roflection at the edge of the Agulhas Bank on the south
coast. The meandering of the Agulhas Current off the
Agulhas Bank creates a semipermanent upwelling cell
centered around Port Alfred on the southeast coast
(Figure 1). This upwelling, along with wind-driven
upwelling during periods of strong and persistent easterly
winds, extends through Algoa Bay and has a lateral range
85–300 km of coastline (Lutjeharms, 2006). The fre-
quency and intensity of upwelling vary seasonally,
with cold, nutrient-rich water being detectable for a
further 2–3 weeks after upwelling events (Goschen et al.,
2015). This region is associated with elevated nutrient
values, with nitrate levels exceeding 20 μmol/L compared
with <5 μmol/L on the adjacent Agulhas Shelf
(Lutjeharms, 2006).
ECOLOGY 3of17
Field sites
To test for the effects of grazing pressure on macroalgal
biomass in upwelling and nonupwelling regions,
grazer-exclusion plots were established at the mid-shore
level on two upwelling (Cape St. Francis −34.211S,
24.837E and Port Alfred −33.613S, 26.889E) and two
nonupwelling shores (Jeffreys Bay −34.026S, 24.931E
and East London −32.955S, 28.005E) on the south
coast of South Africa (Figure 1). Although Jeffreys Bay
and East London do experience occasional periods of
upwelling (<1 upwelling event per month), these periods
are significantly less frequent than at Cape St. Francis
and Port Alfred (≥1 upwelling event per month) and the
sites are referred to as nonupwelling for clarity.
Upwelling regions were chosen based on the literature
(Lutjeharms, 2006; Lutjeharms et al., 2000) and the pres-
ence of permanent or semipermanent upwelling cells was
identified using MODIS aqua chlorophyll asatellite data
obtained from the NASA Earth Data database (tempera-
ture data for each site, including upwelling events, can be
found in Appendix S1: Section S1). Each site differed in
rock formation and structure, with Cape St. Francis
characterized by quarzitic sandstone, Jeffreys Bay by
black shale, compact siltstone, and sandstone, Port
Alfred by quartzite rock formations and East London by
dolerite (Lubke & Moor, 1998). Intertidal communities at
each site were similar in community composition, with
clear zones of Afrolittorina, red algal turf, and mussel
beds moving from the supralittoral fringe to the lower
mid-shore. Mid-shore communities are characterized by
a patchwork of barnacles and limpets, particularly the
large limpet Cymbula oculus, interspersed among
macroalgal communities dominated by Ulva spp.,
Gelidium pristoides and encrusting coralline algae
(Lithophyllum sp. and Lithothamnium sp.). The maxi-
mum tidal range at all sites is ~2 m.
Experimental design
At each site, 15 experimental plots were established in
five blocks around the mid-shore level across ~100 m
of shoreline, with a minimum of 2 m between blocks.
FIGURE 1 Field sites at upwelling (Cape St. Francis and Port Alfred) and non-upwelling (Jeffreys Bay and East London) sites along the
southeast coast of South Africa. Upwelling regions were identified following Lutjeharms et al. (2000).
4of17 GILSON and MCQUAID
Each block contained one replicate from each experimen-
tal treatment. The experiment had a fully factorial design
with two factors: (1) upwelling regime (fixed, two levels:
upwelling and nonupwelling); and (2) grazing pressure
(fixed, three levels: total exclusion, partial exclusion, total
access). Grazer-exclusion plots were established by
enclosing plots with fences (35 × 35 cm, 10 cm high)
constructed from stainless steel mesh (0.9 mm wire diam-
eter, 5.16 mm aperture) fixed to the substratum with
screws and washers. Fences were chosen instead of
enclosed cages with lids to prevent light limitation
(Appendix S1: Figure S2). This allowed the exclusion of
all benthic grazers from the fenced plots. To test for
experimental artifacts affecting macroalgal production as
a result of the presence of the fences, procedural controls
were established using fences around half of the plot in
an L-shape to allow partial grazer access. Experimental
controls were marked at the corner with screws only,
allowing complete grazer access. Fences were cleaned of
any epibiota during every sampling period. Every experi-
mental treatment was replicated five times at each site
but adverse weather and sea conditions meant some
cages were lost and sample sizes varied from three to five
replicates per treatment per site. Prior to the beginning of
the experiment, all experimental and control plots were
scraped clear to ensure all living organisms
were removed and algal and sessile invertebrate cover
was 0%. Plots were left for a 4-week period before surveys
began. The experiment started in January 2021 and was
surveyed monthly for 12 months.
Data collection
To quantify benthic grazing pressure, grazer density was
recorded monthly at each site. Ten 25 × 25 cm quadrats
were placed haphazardly throughout the mid-shore level
and the identity (species level) and density of grazers
were recorded. As grazer size has been shown to be an
important factor in determining the outcome of
algae–grazer interactions, grazers were classified into
meso-grazers and macro-grazers. On South African
shores, dominant macro-grazers in the mid-low inter-
tidal, including the gardening limpet Scutellastra
longicosta and the limpet Cymbula oculus, are large indi-
viduals, >20 mm, and well adapted to wave-exposed con-
ditions (Branch & Odendaal, 2003; Díaz & McQuaid,
2011; Nakin & McQuaid, 2014). Meso-grazers are also
abundant at the mid-shore level and include pulmonate
limpets such as Siphonaria spp. and gastropods including
Oxystele spp. ~15–20 mm in size (Díaz & McQuaid, 2011;
Hodgson, 1999; Whittington-Jones, 1997). As these were
the dominant grazer species identified in the current
study, a 20 mm cut-off between grazer size classes was
chosen to distinguish between meso-grazers and
macro-grazers.
To quantify the effects of grazing pressure and
upwelling regime on the colonization of sessile inverte-
brates, the percentage cover for each sessile invertebrate
species in each plot was estimated monthly using the
point intercept method with a 25 cm × 25 cm quadrat
with 36 intersections, positioned carefully within each
cage to avoid sampling edge effects. Although sedentary
species such as mussels were present during the experi-
ment, abundances were very low (>1 individual per plot)
and invertebrate communities were dominated by sessile
invertebrates (predominantly barnacles). We therefore
refer to sessile, not sedentary, invertebrate communities.
A similar method was used to test for the effects of graz-
ing pressure and upwelling regime on macroalgal per-
centage cover (as a proxy for macroalgal production).
Sessile invertebrates and macroalgae were identified to
species level where possible and species present within
the quadrat but not occurring directly beneath an inter-
section were assigned a percentage cover value of 1%
(O’Connor & Crowe, 2005). The total percent cover
values of macroalgae sometimes exceeded 100% due to
the multistory nature of macroalgal communities.
Grazers found in grazer-exclusion plots during monthly
surveys were removed. At the end of the experiment, bio-
mass was destructively removed from all plots, separated
into species and dried at 60C until constant weight.
To test for the effects of grazing pressure on
macroalgal production, the log response ratio (LRR) was
calculated as a proxy for effect size using paired plots
within each block:
LRR ¼ln %algal covercontrol=%algal covertreatment
ðÞ:
The effect size describes the strength of the grazing
effects inversely; positive values indicate that grazers
promote algal production and negative values indicate
that algal production is reduced (Díaz & McQuaid, 2011).
Before calculating LRR, we tested for experimental
artifacts using the paired differences between the
experimental control and the control in each block. If no
evidence of experimental artifacts was found, estimated
values of percentage cover for control and experimental
control plots were averaged. If artifacts were detected,
only the percentage cover estimates from the experimen-
tal control were used and grazer effects were estimated in
the presence of an artifact. Per capita grazer effects
were then estimated by dividing grazer effects (LRR) by
grazer densities. Last, to test whether the effects of
grazers and upwelling differed between early and
late successional stages of macroalgal communities,
ECOLOGY 5of17
estimates of grazer effects were averaged for the first
three and last three time periods for each experimental
block.
Data analysis
General linear mixed models (LMM) were used to test for
the effects of upwelling regime (fixed, two levels), sam-
pling period (fixed, 12 levels) and site (random and
nested in the upwelling regime, four levels) on total
grazer, meso-grazer and macro-grazer densities. LMMs
were also used to test for the effects of upwelling regime
(fixed, two levels), grazing pressure (fixed, three levels),
sampling period (fixed, 12 levels) and site (random and
nested in upwelling regime, four levels) on sessile inver-
tebrate cover (in percentage), total macroalgal cover and
individual cover of macroalgal species (in percentage),
and total and per capita effect size (LRR). A similar con-
struct was used for macroalgal biomass except for the
exclusion of the sampling period. Last, LMMs were also
used to test for the effects of upwelling regime (fixed, two
levels), successional stage (fixed, two levels) and site
(random and nested in upwelling regime, four levels) on
total effect size (LRR). All main terms and interactions
were included in the model and model selection was
performed using Akaike information criterion (AIC
c
)
values, where the lowest AIC
c
values represented the
optimal model (Zuur et al., 2009). If model assumptions
were met, ANOVA was used to obtain χ
2
and p-values
(package car). When p-values were significant, Tukey
honestly significant difference (HSD) adjusted pairwise
comparisons using least-square means were used for
post hoc comparisons (package lsmeans). Residuals
were visually inspected and QQ plots were used to check
assumptions of normality and homogeneity of variance
(Zuur et al., 2009). When residuals did not meet
model assumptions, data were log-transformed and
the model re-run. All analyses were conducted using
R (R Development Core Team, 2016).
RESULTS
Total grazer density did not differ between upwelling and
nonupwelling sites throughout the survey period
(Figure 2a). However, when separated into meso-grazers
(>20 mm) and macro-grazers (<20 mm), a significant
interaction between the upwelling regime and grazer size
class was identified (Figure 2a,b; Table 1). Specifically,
meso-grazer density was greater at nonupwelling than
upwelling sites but was lower than macro-grazer density
at both upwelling and nonupwelling sites. Macro-grazer
density did not differ between upwelling and
nonupwelling sites (Figure 2inset).
Overall, the sessile invertebrate cover was reduced in
the absence, compared with the presence, of grazers but
was modified by an upwelling regime (Figure 3inset 1;
Table 2). The absence of grazers at nonupwelling sites
reduced sessile invertebrate cover, but there was no effect
of grazing pressure at upwelling sites where cover
remained low. The sessile invertebrate cover also differed
between sampling periods but only at nonupwelling sites,
with the lowest cover in February (austral mid-summer)
and greatest in September (early spring; Figure 3inset 2).
Total algal cover (in percentage) was greater at
upwelling than nonupwelling sites, but only in the
absence of grazers (Figure 4a,b and inset; Table 2). No
effect of the sampling period was identified. There was a
significant effect of the interaction among upwelling
regime, grazing pressure and sampling period on the
cover (in percentage) of the ephemeral Ulva spp.
(Figure 5a,b; Table 2). Specifically, Ulva spp. cover was
greater in the absence of grazers compared with the pres-
ence of grazers but only at upwelling sites. In the absence
of grazers, however, Ulva spp. cover was greater at
upwelling, compared with nonupwelling, sites only dur-
ing February to June and August and September
(i.e., austral late summer to spring). Cover of the late suc-
cessional red alga G. pristoides (in percentage) was
greater in the absence than in the presence of grazers at
both upwelling and nonupwelling sites but did not differ
between grazer treatments within the two levels of
upwelling regime (Figure 5c,d and inset 1; Table 3).
Cover of G. pristoides also differed between sampling
periods but only in the absence of grazers (Figure 4
inset 2; Table 2). Specifically, the cover of G. pristoides
was greater during the last 2 months of the experimental
period (December and January) than in the first two sam-
pling periods (February and March). Total algal biomass
at the end of the experiment was greater in the absence
of grazers, but only at upwelling sites (Figure 6; Table 3).
Grazing effects on macroalgal production were
greater at upwelling than nonupwelling sites
(χ
21,11
=8.018; p=0.004) but did not differ between
sampling periods despite an overall trend of increased
grazer abundance during the austral winter months
(Figure 7a). Although they followed a similar pattern, per
capita grazing effects were not, however, modified by an
upwelling regime or sampling period (Figure 7b). Owing
to high variability, we did not identify any significant
effects of an upwelling regime or successional stage on
the effect size of grazing pressure on macroalgal biomass
(Figure 7c). There was a general trend, however, of grazer
effects being greater at upwelling than nonupwelling sites
for early successional stages, while being similar between
6of17 GILSON and MCQUAID
upwelling regimes for late successional stage macroalgae
(Figure 7c).
DISCUSSION
Our study shows that top-down (grazing pressure) and
bottom-up (upwelling) effects can interact to alter
macroalgal production and highlights the importance of
regional-scale oceanographic processes in understanding
ecosystem functioning in warm-temperate systems. As
predicted, sessile invertebrate cover remained
consistently low at upwelling sites and was reduced at
nonupwelling sites when grazers were excluded.
Macroalgal cover was greater at upwelling sites when
grazers were excluded and there was a strong effect of
succession, with the ephemeral colonizer Ulva spp. domi-
nating species assemblages during early sampling periods
and the late successional species G. pristoides becoming
more abundant toward the end of the experimental
period. In line with ecological theory and our a priori
hypotheses, grazing pressure was greater at upwelling
sites and was greater still during winter months.
Although grazing pressure in early and late successional
FIGURE 2 (a) Total, (b) meso-grazers (<20 mm), and (c) macro-grazers (>20 mm) density (mean ± SE) recorded monthly between
February 2021 and January 2022 at two upwelling (Port Alfred and Cape St. Francis) and two nonupwelling (East London and Jeffreys Bay)
sites along the southeast coast of South Africa. n=6–10. Inset shows meso-grazer and macro-grazer abundance pooled across levels of
sampling period. Lowercase letters represent homogenous groups (p< 0.05) based on Tukey post hoc tests.
ECOLOGY 7of17
stages did not differ statistically, our hypothesis that
grazing pressure would be greater in early successional
stages was partially supported by this general trend.
We have two caveats concerning the interpretation of
our results, however. The first is that we excluded only
benthic grazers and not swimming grazers such as
amphipods or fish. Consequently, we make the implicit
assumption that the densities of such grazers do not dif-
fer between our upwelling regimes. Second, we measure
grazer pressure as density, rather than size (length or bio-
mass). We expect the metabolic rates and energy
demands of grazers to be related to their body sizes and
believe that density is a useful measure of grazing inten-
sity as body size and density are often related. In addi-
tion, the size of the dominant grazers in this study does
not differ significantly between upwelling and non
upwelling sites (Appendix S1: Section S2), indicating that
density may be used as an accurate predictor of grazing
effects in this study.
Sessile invertebrate cover, dominated by barnacle spe-
cies (predominantly Chthamalus spp.), was reduced at
upwelling sites, probably as a result of the dominance of
the ephemeral Ulva, which exhibits rapid growth under
conditions of increased nutrient levels, allowing it to
dominate available space through its rapid growth
(Dungan, 1986; Sousa, 1979). The establishment and
rapid growth of algal propagules, with growth presum-
ably being much faster under upwelling conditions, pre-
vent sessile invertebrate recruitment and establishment
resulting in barnacles losing the competition for space
(Hawkins, 1983; Sousa, 1979). This suggestion is
supported by the reduced sessile invertebrate cover at
nonupwelling sites in the absence of grazers, with a lack
of grazing pressure allowing rapid colonization and the
establishment of algal propagules (Dungan, 1986).
Moreover, barnacle recruitment has been linked previ-
ously to water temperature, with warmer temperatures
resulting in increased recruitment (Blanchette et al.,
2006). Given that upwelling water temperatures are sig-
nificantly lower than ambient sea surface temperature
(SST), it is likely that a combination of lower SST and
rapid growth of ephemeral algae limited barnacle recruit-
ment under upwelling conditions. Although it has been
suggested that higher phytoplankton availability
increases barnacle reproduction and larval supply
(Leslie et al., 2005), it is likely that during periods of
heavy upwelling, offshore advection of larvae limits
larval supply in species with dispersive larvae, which
is the dominant mechanism of larval dispersal for inver-
tebrate communities in this region (Blanchette et al.,
2006; Broitman et al., 2001; Connolly et al., 2001;
Shkedy & Roughgarden, 1997).
We identified greater macroalgal cover at upwelling
sites in the absence of grazers. This reflects the conse-
quences of alteration to both bottom-up and top-down
effects. In grazer-exclusion treatments, enhanced nutrient
availability during upwelling events leads to increased
algal growth rates and the release of macroalgae from
top-down control (Blanchette et al., 2006; Bustamante
et al., 1995). Increased macroalgal cover was driven by
the ephemeral green algae Ulva spp., with a clear pattern
of succession throughout the experimental period. Ulva is
a fast growing, opportunistic foliose species that is able to
reproduce throughout the year, making it a perfect early
colonizer of available space, particularly under increased
nutrient supply such as upwelling conditions. During the
winter months, however, due to more efficient utilization
of resources and greater competitive ability, the late suc-
cessional red colonizer G. pristoides outcompeted the
ephemeral green and dominated plots by the end of
the experimental period. The macroalgal cover did not
differ between upwelling regimes in the presence of
grazers, confirming that grazers exert significant
top-down control over macroalgal production and any
increases in macroalgal productivity resulting from
bottom-up effects at upwelling sites were not sufficient
enough to overwhelm top-down control (Nielsen, 2001).
Moreover, this result does not support the idea that cold
upwelled water imposes metabolic constraints on grazers
and reduces grazing activity, thereby weakening
top-down effects (Bruno et al., 2015; Kishi et al., 2005). It
is difficult, however, to disentangle the relative effects of
nutrient input and cooling on grazing activity and their
subsequent effects on macroalgae given that these effects
act simultaneously and are driven by the same processes
(but see Thompson et al., 2004). Few studies have focused
on using manipulative experiments to disentangle these
effects, with the exception of grazing effects on early suc-
cessional macroalgal community composition (Masterson
et al., 2008) and microbial biomass (Thompson et al.,
2004) on rocky shores. Mesocosm experiments are
needed to disentangle these effects and assess their
impact on ecological processes and functioning.
TABLE 1 Linear mixed effects models of sampling period,
upwelling regime and grazer size on the abundance of meso-grazers
(<20 mm) and macro-grazers (>20 mm) surveyed at upwelling and
nonupwelling sites on the southeast coast of South Africa.
Source of variation X
2
df p-value
Sampling period, SP 29.88 11 0.001
Upwelling regime, UR 4.64 1 0.03
Size, S 910.43 1 <0.001
UR × S 121.04 1 <0.001
Note: Significant terms are highlighted in bold ( p< 0.05).
8of17 GILSON and MCQUAID
Contrary to other published literature (Sellers et al.,
2020), but in line with ecological theory, we identified
greater grazing pressure under upwelling conditions.
Meso-grazer abundance was greater at nonupwelling
sites but previous studies have shown weak effects by
meso-grazers (Poore et al., 2009) and, in the current
study, the greatest meso-grazer densities were lower than
even the lowest macro-grazer densities. Although there
was a trend toward greater macro-grazer abundance
under upwelling conditions, macro-grazer abundance did
not differ significantly between upwelling regimes due to
large variability in the dataset. Such results are common
on rocky shores where species distribution can be patchy
and is determined by bottom-up, top-down, and commu-
nity processes. For example, while grazers with
crawl-away larvae often respond to local levels of
FIGURE 3 Sessile invertebrate cover (in percentage) in the (a) absence and (b) presence of grazers (mean ± SE) from experimental
plots surveyed monthly between February 2021 and January 2022 at two upwelling (Port Alfred and Cape St. Francis) and two nonupwelling
(East London and Jeffreys Bay) sites along the southeast coast of South Africa. n=6–10. Insets 1 and 2 show sessile invertebrate cover
(in percentage) pooled across levels of grazing pressure and sampling period, respectively. *Represents distinguishable groups (p< 0.05)
based on Tukey post hoc tests.
ECOLOGY 9of17
TABLE 2 Linear mixed effects models of upwelling regime and grazing pressure on sessile invertebrate cover, total algal cover, cover of
Ulva spp. and Gelidium pristoides (in percentage) in experimental plots at upwelling and nonupwelling sites on the southeast coast of South
Africa.
Source of variation df
Invertebrates Total Ulva spp. Gelidium pristoides
χ
2
pχ
2
pχ
2
pχ
2
p
Sampling period, SP 11 21.82 0.025 3.72 0.97 19.38 0.05 15.05 0.17
Upwelling regime, UR 1 0.36 0.544 3.42 0.06 4.03 0.044 0.09 0.75
Grazing pressure, GP 1 14.1 <0.001 497.38 <0.001 545.20 <0.001 72.39 <0.001
SP × UR 11 20.15 0.04 7.3 0.77 40.47 <0.001 6.83 0.81
SP × GP 11 4.68 0.94 6.97 0.8 59.56 <0.001 36.82 0.001
UR × GP 1 4.32 0.03 59.84 <0.001 206.22 <0.001 6.85 0.008
SP × UR × GP 11 5.13 0.92 57.90 <0.001 8.95 0.62
Note: Significant terms are highlighted in bold ( p< 0.05).
FIGURE 4 Total macroalgal cover (in percentage) in the (a) absence or (b) presence of grazers (mean ± SE) from experimental plots
surveyed monthly between February 2021 and January 2022 at two upwelling (Port Alfred and Cape St. Francis) and two nonupwelling
(East London and Jeffreys Bay) sites along the southeast coast of South Africa. n=6–10. Inset shows total algal cover (in percentage) pooled
across levels of sampling period. Lowercase letters represent homogenous groups (p< 0.05) based on Tukey post hoc tests.
10 of 17 GILSON and MCQUAID
FIGURE 5 Total cover (in percentage) of Ulva spp. (a, b) and Gelidium pristoides (c, d) in the absence (a, c) and presence (b, d) of
grazers (mean ± SE) from experimental plots surveyed monthly between February 2021 and January 2022 at two upwelling (Port Alfred and
Cape St. Francis) and two nonupwelling (East London and Jeffreys Bay) sites along the southeast coast of South Africa. n=6–10.
Insets 1 and 2 show total cover (in percentage) of G. pristoides pooled across levels of upwelling regime and sampling period, respectively.
*Represents distinguishable groups (p< 0.05) based on Tukey post hoc tests.
ECOLOGY 11 of 17
predation (Wieters et al., 2008), almost all of the species in
this region have dispersive planktonic larvae and offshore
advection may have prevented local recruitment to upwell-
ing sites. Local predator abundance may also have differed
between upwelling and nonupwelling sites, driving differ-
ences in grazer density via top-down effects (Branch, 1978;
Branch & Cherry, 1985). It is more likely, however, that
given a larger sample size than was logistically possible in
this study, significantly greater macro-grazer densities at
upwelling sites would have been identified. Per capita
effects did not show any significant effects due to high var-
iability in the dataset but followed the same general pat-
tern as overall grazing effects, suggesting that the
dominance of macro-grazers over micro-grazers at upwell-
ing sites results in a larger individual impact as shown by
Nielsen and Navarrete (2004).
Although we did not measure grazer size continuously
throughout the experimental period, we did not identify
any significant differences in body size between the most
abundant grazer species at upwelling and nonupwelling
sites during post hoc sampling (Appendix S1:SectionS2).
This further supports the idea that greater grazing pressure
at upwelling sites is driven by greater densities of
macro-grazers. Body size is inversely related to population
densities in many systems and has been shown to correlate
positively with foraging time, handling time and consump-
tion rates (Navarrete & Menge, 1997;Woodetal.,2010).
Greater macroalgal production at upwelling sites supports
the idea that these areas are able to support larger individ-
ual grazers through greater food quality and availability,
thereby controlling the grazer population via bottom-up
effects (Bosman et al., 1987; Pulgar et al., 2013). Greater
size and biomass of dominant intertidal grazers in areas of
high upwelling activity have previously been reported for
South African shores, with maximum biomass and shell
length of dominant grazers positively related to in situ pro-
ductivity (Bustamante et al., 1995). In addition, the high
diversity of grazers in South Africa includes species that
exploit both tide-in and tide-out grazing windows, poten-
tially maintaining a constant level of increased top-down
control due to the exploitation of complementary
resources (Branch & Cherry, 1985). It is important to
remember, however, that interactions between top-down
control and bottom-up forcing can be modified both
directly and indirectly by physical processes and our
results may not be consistent across gradients of zonation
or wave exposure (Díaz et al., 2011; Díaz & McQuaid,
2011; Jonsson et al., 2006). Future studies should focus on
understanding the relationship between upwelling and
herbivore demography and behavior to disentangle how
regional-scale processes are linked to local-scale processes.
When nutrient levels are high under upwelling condi-
tions, high productivity and growth rates of foliose species
have been reported to overwhelm top-down control and
weaken grazing pressure in early successional stages
(Nielsen, 2001;Sellersetal.,2020). Although not signifi-
cant, grazer effects (measured as effect size) at upwelling
sites in the current study were greater in early successional
stages, indicating heavy grazing on the ephemeral green
Ulva spp. that dominated at the beginning of the experi-
ment. In contrast, however, grazing pressure was reduced
on late successional algal species, dominated by
G. pristoides, that have better grazing defenses and proba-
bly reach refuge in size (Aguilera & Navarrete, 2012;
Nielsen & Navarrete, 2004). Changes in consumer effects
through community succession have previously been dem-
onstrated as reflecting changes in functional traits of the
dominant algal species such as growth rate, productivity,
resistance and tolerance to herbivore damage and con-
sumption and individual size (Aguilera & Navarrete, 2012).
It is important to consider, however, that changes in
TABLE 3 Linear mixed effects models of upwelling regime
and grazing pressure on the total remaining biomass (in grams) in
experimental plots at upwelling and nonupwelling sites on the
southeast coast of South Africa.
Source of variation χ
2
df p-value
Upwelling regime, UR 6.82 1 0.009
Grazing pressure, GP 28.22 1 <0.001
UR × GP 7.67 1 0.005
Note: Significant terms are highlighted in bold ( p< 0.05).
FIGURE 6 Total macroalgal biomass (in grams; mean ± SE)
from experimental plots surveyed between February 2021 and
January 2022 at two upwelling (Port Alfred and Cape St. Francis)
and two nonupwelling (East London and Jeffreys Bay) sites along
the southeast coast of South Africa. n=6–10. The upper and lower
boundaries of each box represent the 75th and 25th percentiles,
respectively, and the line in the middle represents the median.
Upper and lower whiskers represent the 90th and 10th percentiles,
respectively. Lowercase letters represent homogenous groups
(p< 0.05) based on Tukey post hoc tests.
12 of 17 GILSON and MCQUAID
functional traits in consumers such as feeding guild may
also contribute to changes in grazing pressure throughout
theexperiment.Forexample,somegrazersareableto
remove spores and algal germlings during early coloniza-
tion but cannot consume the same species once they reach
a refuge in size, thereby reducing top-down control of the
same species at later successional stages (Aguilera &
Navarrete, 2012;Jonssonetal.,2006;Lubchenco,1982,
1983; Nielsen & Navarrete, 2004).
Although studies specifically designed to test grazing
effects across upwelling regimes are scarce, current data
for cold-temperate and tropical systems has identified
greater top-down control of production in areas of
nonupwelling (Sellers et al., 2020). These systems, how-
ever, do not experience the dramatic fluctuations in air
and sea temperatures found in warm-temperate systems
where SST during upwelling events can be 11C while
rock surface temperatures can regularly reach above
40C (Appendix S1: Section S1) during aerial exposure.
Such dramatic temperature fluctuations have the poten-
tial to drive significant changes in the metabolic rates of
grazers, thereby altering consumer–resource interactions
and top-down control (Miller et al., 2014;O’Connor, 2009;
Pincebourde et al., 2008). During emersion, high aerial
FIGURE 7 Total (a) and per capita (b) grazing effects (log response ratio [LRR]) on macroalgal communities and total grazing effects
(LRR) on macroalgal community successional stage (c) found in experimental plots surveyed monthly between February 2021 and January 2022
at two upwelling (Port Alfred and Cape St. Francis) and two nonupwelling (East London and Jeffreys Bay) sites along the southeast coast of
South Africa. n=6–10.
ECOLOGY 13 of 17
temperatures can drive species past their optimal temper-
ature range, increasing metabolic demand, and requiring
energetically costly adaptations, such as heat shock pro-
tein production, that can result in detrimental physiologi-
cal effects (Dong & Williams, 2011; Miller et al., 2009). In
the intertidal, where foraging time is limited to periods of
immersion, it may not be possible to consume enough
food to compensate for the negative effects of high tem-
peratures. Under upwelling conditions, cold upwelled
waters may offset the negative effects of increased tem-
perature during emersion, limiting the detrimental effects
of increased metabolic demands and enabling greater
growth and reproduction (Blanchette et al., 2007). In
addition, a greater food supply at upwelling sites may be
sufficient to compensate for an increase in the grazing
effort required to sustain greater metabolic demand and
increase growth rates, strengthening top-down control
(Blanchette et al., 2007; Gilman, 2006; Miller et al., 2015;
O’Connor, 2009). Warmer temperatures under conditions
of limited food supply have been associated with lower
growth and reproduction for several species of limpets,
mussels, barnacles and oysters (Blanchette et al., 2007;
Gilman, 2006; Gilson et al., 2021; Miller et al., 2015;
Sanford & Menge, 2001).
In contrast, however, it has been hypothesized that cold,
upwelling waters depress the metabolic rates of consumers,
reducing top-down control in upwelling regions (Sellers
et al., 2020). Higher aerial temperatures may have the oppo-
site effect during upwelling events, allowing the mainte-
nance of higher metabolic rates during periods of upwelling
and increasing top-down control. The positive effects of
increased food supply in upwelling regions can be dimin-
ished by the negative influence of low SSTs on growth,
supporting the idea that warmer aerial temperatures may
help mitigate temperature effects and lead to an overall pos-
itive effect on growth (Blanchette et al., 2007). Gastropod
grazers have been shown to alter foraging behavior when
exposed to temperature stress and may choose to graze dur-
ing warmer air temperatures when the tide is out to coun-
teract the negative effects of cold upwelling periods
(Branch & Cherry, 1985;Gray&Hodgson,1998; Little,
1989; Williams & Morritt, 1995). In addition, high aerial
and SSTs that reduce the performance of intertidal limpets
under low food availability have been shown to be less det-
rimental under high food availability, indicating that the
negative effects of high temperatures are strongest with lim-
ited food supply (Gilman, 2006). The body temperatures of
intertidal animals, a measurement that reflects the influ-
ence of seawater temperature during immersion and body
temperature during aerial exposure, have previously been
positively correlated with growth (Blanchette et al., 2007;
Thompson et al., 2000). It is difficult, however, to decouple
the effects of both aerial and aquatic temperatures on
metabolic rates and energy demand and detailed experi-
ments are needed to isolate the relative effects of aerial and
aquatic temperatures and theirinteractionwithfoodsup-
ply. Furthermore, responses can be species-specific and
change with population demography.
In summary, we show that changes to both top-down
and bottom-up pressures can alter patterns of primary pro-
duction in rocky intertidal habitat, but that the results for
our warm-temperate system do not follow those for
cold-temperate or tropical systems. We highlight how com-
munityprocessessuchassuccessioncanaltertheeffectsof
top-down and bottom-up pressures so that they are not
uniform through time. Given that we did not exclude
higher consumers such as crabs and fish that can also graze
algae, we in fact underestimate grazing pressure and show
that excluding even a single group of grazers can signifi-
cantly alter algae–grazer interaction strengths. As the west
coast of South Africa is cold temperate, there is a unique
opportunity to gain valuable insights into the driving
mechanisms behind the observed differences in our
warm-temperate system and the cold-temperate and tropi-
cal literature. Future studies should focus on investigating
the interaction between grazing pressure and upwelling in
this cold-temperate bioregion to identify whether differ-
ences in the strength of top-down control in this study are
due to regional (i.e., South African) or larger scale pro-
cesses. Under future climate change conditions, ocean
warming is predicted to increase primary productivity and
reduce metabolic constraints imposed on herbivores so that
detailed mesocosm experiments that decouple the effects of
temperature and upwelling on both macroalgae and
grazers will be especially informative. Disentangling these
effects and their interactions, as well as identifying individ-
ual species responses, is critical to understanding the
knock-on effects on food-web dynamics and ecosystem
functioning.
ACKNOWLEDGMENTS
We thank Jaqui Van Dyk, Garyn Delport, Abigail
Wolmerans, and Dr. Natanah Gusha for their invaluable
help in the field. This study was funded by a fellowship
from Rhodes University and the National Research
Foundation.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.
DATA AVAILABILITY STATEMENT
Data (Gilson & McQuaid, 2023) are available in Dryad at
https://doi.org/10.5061/dryad.3j9kd51qz.
ORCID
Abby R. Gilson https://orcid.org/0000-0003-4607-1376
14 of 17 GILSON and MCQUAID
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SUPPORTING INFORMATION
Additional supporting information can be found online
in the Supporting Information section at the end of this
article.
How to cite this article: Gilson, Abby R., and
Christopher McQuaid. 2023. “Top-Down versus
Bottom-Up: Grazing and Upwelling Regime Alter
Patterns of Primary Productivity in a
Warm-Temperate System.”Ecology 104(12): e4180.
https://doi.org/10.1002/ecy.4180
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