Perspectives in Phycology, Vol. 2 (2015), Issue 1, p. 11–30
Published online February 2015
The responses of brown macroalgae to environmental change
from local to global scales: direct versus ecologically mediated effects
Martin Wahl
1
*, Markus Molis
2
, Alistair J. Hobday
3
, Steve Dudgeon
4
, Rebecca Neumann
5,6
,
Peter Steinberg
5,6
, Alexandra H. Campbell
5,6
, Ezequiel Marzinelli
5,6
& Sean Connell
7
1
GEOMAR Helmholtz Centre for Ocean Research, Duesternbrookerweg 20, 24105 Kiel, Germany
2
Section Functional Ecology, Alfred Wegener Institute, Helmholtz Zentrum für Polar- und Meeresforschung, Am
Handelshafen 12, 27570 Bremerhaven, Germany
3
CSIRO Oceans and Atmosphere Flagship, Hobart, Tasmania, 7000, Australia.
4
California State University, Northridge, Ca 91330–8303, USA
5
Centre for Marine Bio-Innovation and School of Biological, Earth and Environmental Sciences, University of
New South Wales, Sydney, NSW 2052, Australia
6
Sydney Institute of Marine Science, 19 Chowder Bay Rd, Mosman, Sydney, NSW 2088, Australia
7
Southern Seas Ecology Laboratories, University of Adelaide, South Australia, Australia
*Corresponding author: mwahl@geomar.de
With 2 gures
Abstract: In many temperate regions, brown macroalgae full essential ecosystem services such as the provision of structure, the xation
of nutrients and carbon, and the production of biomass and oxygen. Their populations in many regions around the globe have declined and/
or spatially shifted in recent decades. In this review we highlight the potential global and regional drives of these changes, describe the
status of regionally particularly important brown macroalgal species, and describe the capacity of interactions among abiotic and biotic
factors to amplify or buffer environmental pressure on brown macroalgae. We conclude with a consideration of possible management and
restoration measures.
Keywords: Ascophyllum, Ecklonia, Fucus, Laminaria, Macrocysis, disease, kelp, climate change, eutrophication, multi-factorial change,
ecological modulation, phaeophyta
1. Introduction
Anthropogenic activities have triggered environmental
changes that greatly exceed the natural (Rockstrom et al.
2009, Steffen et al. 2011, section 3). The speed of change
in average environmental conditions and the increased fre-
quency of extreme events (heat waves, hypoxia) may exceed
the potential of marine organisms for tolerance or adaptation
(IPCC-AR5 2014, Koehn et al. 2011). Large-scale climate
changes also interact with various regional-scale stressors.
The compound effects of stressors may be additive, antago-
nistic or synergistic, but tend to be synergistic (“unexpect-
edly strong”) with increasing number of co-acting stressors
(Crain et al. 2008, Brown et al. 2013).
Many marine populations are responding to global
change (comprising climate change, shipping but also
regional changes in coastal development, pollution or sh-
ing; reviewed by Firth & Hawkins 2011, see section 4) with
changes in distribution, abundance, physiology and phenol-
ogy (e.g. Parmesan & Yohe 2003, Poloczanska et al. 2013).
Retreating and advancing range margins, and contracting
and fragmenting ranges are well documented in terrestrial
systems, but are much less commonly reported from the
marine realm-particularly for the ecologically important
brown macroalgal species (e.g. Hawkins et al. 2009, and ref-
erences therein). Ongoing and expected changes in seaweed
communities are relevant since seaweed-dominated habitats
are hotspots of biodiversity, represent the bases of numer-
ous food webs and provide valuable ecosystem services
(Wernberg et al. 2011a, Harley et al. 2012b).
Seaweeds may be particularly sensitive to global change
because they are sessile, with limited propagule dispersal (but
see Hobday 2000, Thiel & Gutow 2004, Coleman et al. 2011)
and sensitive to temperature (Breeman 1988, Eggert 2012)
© 2015 The authors
DOI: 10.1127/pip/2015/0019 E. Schweizerbart´sche Verlagsbuchhandlung, Stuttgart, Germany, www.schweizerbart.de
Open Access Article
12 M. Wahl et al.
because unlike many heterotroph species they may not escape
global warming by retreating into deeper (cooler but darker)
waters. Seaweeds directly respond to most of the variables
affected by global change (e.g. photon ux density, tempera-
ture, nutrients) in addition to being indirectly affected by shift-
ing demographic processes such as competition, consumption,
parasitism and fouling (Wahl et al. 2011, Harley et al. 2012b,
Koch et al. 2013). Such sensitivities have been expertly
reviewed by Harley and co-workers (2012b) while Koch and
colleagues (2013) have covered the interactive impacts of
warming and acidication on macroalgal physiology.
Observed large scale range shifts of macroalgae represent the
integrated response to multiple and interactive stress (abiotic
and biotic) on all ontogenetic stages of a species (e.g.Hawkins
et al. 2009, Harley et al. 2012b) although patterns may differ
remarkably between taxa and regions (e.g. Lima et al. 2007,
Nicastro et al. 2013, Wernberg et al. 2011a). Regional dissimi-
larity in response patterns may result from differences in the
interactions between local and global stressors and/or be due
to abiotic changes being differently amplied or buffered by
shifts in competition, consumption, parasitism, epibiosis, or
diseases in the various ecosystems. In particular, the ecologi-
cal modulation of environmental stress is poorly understood.
To help ll the gap between cause and effect (e.g. physiologi-
cal sensitivity as a proximate “cause” and range shifts as an
“effect”) we here present several illustrative regional case
studies of brown macroalgae (Fig. 1) under global change
pressure. In contrast to the aforementioned reviews on mac-
roalgae in a changing world, we strive to differentiate between
global and regional scale pressures and highlight the impor-
tance of stress modulation by biotic interactions. To achieve
this, we describe in detail the state and prospects for important
habitat-forming brown algal species from various biogeo-
graphic regions around the globe. We then summarize the sug-
gested direct and indirect pressures in these macroalgal
communities to highlight the potential for connected buffering
and amplifying feed-back loops among biotic and abiotic
stresses on macroalgae. We particularly emphasise the indirect
effects, i.e. the mediation of abiotic stress via shifting biotic
interactions. This aspect of ecological modulation of global
change impacts is very poorly known even as it becomes ever
more apparent that such indirect effects may outweigh the
direct effects of, for instance, warming or acidication (e.g.
Harley et al. 2012b). Finally, we consider the range of man-
agement options for reversing declines of impacted macro-
algal populations in a changing world.
2. Potential pressures on macroalgae
2.1 Abiotic pressures
Increased human populations, particularly in coastal regions,
have resulted in intensication of existing, as well as the
emergence of new algal stressors, including coastal eutroph-
ication, hypoxia (Keeling et al. 2010), invasive species
(Sutherland et al. 2014), disease (Sutherland et al. 2014),
and anthropogenic climate change (IPCC-AR5 2014). The
climate-related change in physicochemical properties of the
environment has been thoroughly reviewed and will not be
covered here (e.g. IPCC 2013, Graewe et al. 2013, Doney et
al. 2012). In brief, climate change results in a range of effects
on the ocean including precipitation and runoff changes, and
temperature and circulation changes, while the direct effects
of ocean acidication are just beginning to be revealed by
a range of observational and experimental studies (Doney
et al. 2012). These anthropogenic stressors, many with a
Fig. 1. Global distribution of the major brown macroalgae species treated in this review [after
Steneck & Johnson 2013, in: Bertness, M.D. et al. (2014), Marine Community Ecology and
Conservation, Sinauer; GBIF and personal observation of the authors].
Responses of brown macroalgae to environmental change from local to global scales 13
long-term trend, compound an existing natural set of oscilla-
tions at a range of time scales from short-term storm events
to annual and decadal climate uctuations (e.g. ENSO,
PDO) that inuence the performance of brown macro-
algae. Climate variability has been an important factor in
many studies on brown algae, particularly in understanding
environmental stress – e.g. ENSO, temperature and nutrient
availability impacting Macrocystis in California (Dayton et
al. 1984). Insights from climate variability are also useful
guides to the long-term change that may occur over coming
decades. As an example, natural experiments with CO
2
seeps
are providing a window into the performance of algae in an
“acidic” ocean (Hall-Spencer et al. 2008).
Model projections to 2100 and beyond strongly suggest
that pH will decline further, ocean temperatures will rise in
most places, and extremes will become more frequent (IPCC
2013). The rate of warming, but presumably also the shift in
other physical variables, varies among seasons and regions
(e.g. Graewe et al. 2013, IPCC 2013, BACC 2010, Hobday
& Pecl 2014). Direct CO
2
impacts tend to be negative for
crustose coralline algae but positive for eshy macrophytes
(Koch et al. 2013), but there are also implications of ocean
acidication for the grazers of brown algae (urchins), and the
early life history stages of many brown algae (Gaitán-Espitia
et al. 2014). Too little work has been done on the different
life stages of seaweeds or with multiple stressors to allow a
clear picture to emerge (e.g. Wahl et al. 2011).
Coupled with increasing areas of anoxic waters and
coastal eutrophication, the outlook for coastal temperate
systems is poor, with dramatic changes in macroalgal com-
munities likely (Nellemann et al. 2008). Changes in indirect
inuences – e.g. nutrient supply, mixing, and grazing pressure
are less certain, and model results of algal impact to date are
conicting. Overall, given the rate of change and compound-
ing of algal stressors, we consider the probability for long-
term impact is substantial. We show in subsequent sections
that declines in single species are expected, with subsequent
changes in community structure and composition likely, but
less predictable (e.g. Wernberg et al. 2011b). For example,
dramatic shifts in algal distributions attributed to coastal
warming are reported for eastern Australia, where 85% of
seaweed species had shifted south in the period 1990–2009
compared to 1940–1960, while 56% on the west coast were
recorded farther poleward (Wernberg et al. 2011a). Extreme
events, particularly storms and marine heat waves also result
in dramatic and large changes in distribution (Wernberg et al.
2012). In the following sub-sections, we detail responses to
a range of regional stressors including coastal development,
herbivory, competition and disease.
2.2 Coastal development
Human-driven environmental changes through coastal
development are producing combinations of environmental
conditions that may push many ecological systems outside
the environmental envelope in which they evolved. Indeed,
there is an increase in reporting of algal-dominated transi-
tioning to contrasting states under altered environmental
conditions (Airoldi et al. 2008). Some of the most striking
of these occur in kelp forests which transition from a topo-
graphically complex, productive and diverse system to con-
trasting system of algae with topographic simplicity, lower
diversity and productivity. These transitions from kelps to
turf-dominated landscapes or algal mats occur in Norway,
Sweden, Baltic, Mediterranean, Gulf of Maine, Australia and
New Zealand (section 4.3).
A common feature associated with these changes is a degra-
dation of water quality that is enriched with resources, particu-
larly nutrients in the form of nitrogen from land-based activities
(e.g. catchment management, wastewater treatment plants).
Change of resource availability has long been known to play
a fundamental role in regulating the productivity of individu-
als, species and, ultimately, communities (Harpole et al. 2011),
but we are only just beginning to understand the implications of
local activities that modify small-scale conditions and how they
will combine with change in global conditions.
Resource enhancement is particularly problematic for the
stability of algal dominated systems because they can trans-
form normally subordinate algae to become ecological dom-
inants. The very reason why ‘kelp-turf phase-shift’ tends to
occur mostly on polluted coasts is because the altered water
conditions favour a suite of species, which due to their physi-
ology (i.e. fast uptake of nutrients) and life history (ability to
withstand high sediment loads) are well suited for polluted
environments. The increase in carbon emissions and take-up
by the oceans represents carbon enrichment on a global scale
and has the potential to interact with coastal development
to accelerate change (Russell et al. 2009). Unlike nitrogen
enrichment, which tends to be localised and occur on rela-
tively rapid timescales of years to decades, carbon enrich-
ment occurs on biogeographic scales and accumulates more
slowly. Hence, the nature of stasis or change within the next
100 years will depend on interactions between local through
global scale change in environmental conditions. For exam-
ple, nitrogen enrichment on some coasts likely increases
the probability of community change, but for many coasts
without nutrient pollution the enrichment of carbon alone
may be insufcient to drive community change. Moreover
the impact of resource enrichment will vary among species,
potentially leading to shifts in species dominance that reects
species-specic limitations through contrasting physiolo-
gies (Falkenberg et al. 2013). As human activities modify
resource availability at different scales and places, some spe-
cies may be released from these limitations while others may
not be, potentially bringing considerable variability in the
nature of change across the world’s rocky coasts.
Further changes in the coastal environment linked to
human activity such as littoral constructions providing new
hard substratum, changes in current regime, suspended matter
and sedimentation rates (e.g. Bulleri & Chapman 2010), shifts
in shing pressure and disturbances linked to increasing
14 M. Wahl et al.
Fig. 2. Effects of some global change variables (grey) affecting the target macroalga (green) directly or indirectly via shifts in biotic
interactions (orange). The conceptual scheme is incomplete, merely qualitative and mainly intended to illustrate the potential for amplify-
ing and buffering feed-back loops. Many but not all of the effects depicted are described in the text and referred to by the effect numbers
of this graph. A = defense production, B = growth and reproduction, C = light harvesting, AG = anti-grazer defense, AF = anti-fouling
defense. Digits = direct effect on or from the target macroalga. 1: shading lowers light harvest; 2: eutrophication may increase competi-
tiveness; 3: shading epibionts will reduce light harvest; 4: grazing reduces biomass and, thus, net growth, reproduction and light harvest-
ing; 5: diseases reduce fitness (growth, reproduction); 6: warming reduces fitness of brown alga at their equator-ward range margin;
7: competition reduces fitness; 8,9: defenses may limit the effects of grazing and fouling. Letters = interaction among potential stressors.
a: enhanced growth increases competitiveness; b: grazing may reduce the degree of fouling; c,d,e,f: bioinvasions may increase the
numbers of pathogens, grazers, epibionts and competitors; g, h: warming tends to enhance grazing and fouling pressure, i: warming
favors invasions; j,k: eutrophication favors ephemeral algal competitors (plankton, filamentous algae) and epiphytism, l: acidification
favors non-calcifying over calcifying competitors, m: acidification may reduce grazing of calcifying consumers
tourist activities may reduce the habitat quality for macro-
algae but will not be treated in detail here.
2.3 Herbivory
In marine habitats, the removal of biomass by grazers (inter-
action “4” in Fig. 2) affects plant biomass stronger than in
terrestrial habitats. This is due to a higher per capita effect of
marine grazers (Cyr & Pace 1993) and a higher availability
of seaweed biomass for grazers, because seaweeds often lack
structural elements and, unlike terrestrial plants, lack below-
ground biomass (Hay 1991). Marine herbivores reduce, on
average, 68% of the abundance of primary producers world-
wide (Poore et al. 2012). Strongest grazing effects were
reported for rocky intertidal shores, while habitats dominated
by vascular plants showed the weakest effects (Poore et al.
2012). On tropical coasts 50 to 100% of seaweed production
Responses of brown macroalgae to environmental change from local to global scales 15
is often consumed, mainly by herbivorous shes (Hay 1997),
while urchin grazing may denude kelp beds at boreal to polar
latitudes (e.g. Norderhaug & Christie 2009), indicating that
grazing by macro-herbivores is a major stressor for seaweeds
at all latitudes. Yet, herbivores rarely consume individual
seaweeds entirely. This allows seaweeds to respond to graz-
ing and to persist by either compensating grazing-induced
biomass loss with growth or by deterring grazers (“8” in
Fig. 2; Cronin 2001). As a consequence of this seaweed
persistence, meso-herbivores also use seaweeds on which
they feed as a habitat and nursery ground. This spatially
close association between meso-herbivores and seaweeds
makes strong species interactions and co-evolution possible.
The grazing activity of meso-herbivores, for instance, may
indirectly affect seaweed performance and tness because
thallus damage can increase seaweed susceptibility to dis-
eases (“p” in Fig. 2; see B5). Moreover, feeding scars in the
thallus surface of tough seaweeds may facilitate consump-
tion by grazing species that have difculties in penetrating
undamaged thallus parts (Molis et al. 2010). Epibionts may
enhance or reduce the consumption of the host alga depend-
ing on the identity of the grazer (Karez et al. 2000) and the
epibionts (“n” in Fig. 2; Wahl & Hay 1995). On the other
hand, grazing can be advantageous for seaweeds, because
some grazers remove competing epiphytes (“o” in Fig. 2; see
C4) without consumption of the underlying seaweed thallus,
which receives more light and nutrients after the removal of
the epiphytes (Underwood et al. 1992).
Besides biotic factors, environmental characteristics
may affect seaweed accessibility and palatability for graz-
ers. Exposure to ultraviolet radiation (UVR), for instance,
induced higher levels of UVR-blocking phlorotannins in
the brown seaweed Fucus vesiculosus and stimulated con-
sumption by the isopod Idotea granulosa (Pavia et al. 1997).
Furthermore, chemical anti-herbivory defences are affected
in some macroalgae by irradiance and temperature (“1” &
“6” in Fig. 2; see 4.1). Moreover, wave exposure may shift
isopod consumption among Fucus species, because isopods
were able to attach better to the narrow-leafed F. vesiculosus
than to its broad-leafed congener F. serratus (Engkvist et al.
2004). In addition, thallus toughness may be higher on wave-
exposed than on wave-sheltered shores, which also affects
grazing impact (M Molis, unpubl. data).
Several anthropogenic factors are likely to increase rather
than decrease grazing impact in a future ocean. First, cas-
cading effects of overshing may lead to stronger grazing
pressure on seaweed assemblages, because of the reduced
top-down control of (meso-)grazers. Second, ongoing deple-
tion of stratospheric ozone will increase future irradiance
of UVB radiation particularly in intertidal habitats, which
may increase the consumption of seaweeds by herbivores
like Idotea granulosa (Pavia et al. 1997). Third, native her-
bivores may provide biotic resistance to plant invasions
(Parker & Hay 2005), but the arrival of non-indigenous
herbivores eliminates this ecosystem service (Parker et al.
2006), which may strongly affect the species composition of
the macrophytobenthos of recipient habitats. Fourth, effects
of ocean acidication may weaken the calcareous anti-
herbivory mechanism of certain seaweeds, but may not affect
palatability of non-calcied seaweeds (“m” in Fig. 2; Gutow
et al. 2014). Yet in combination with adverse effects on cal-
cied herbivores and higher temperatures, ocean acidica-
tion may cause shifts from kelp to algal turfs (“l” in Fig. 2;
Connell & Russell 2010, see 3.2 & 4.3). Finally, in a warmer
ocean we should expect an increase in grazing impact due
to higher metabolic activities (“g” in Fig. 2), reduced herbi-
vore defences (“6” –> “8” in Fig. 2; Weinberger et al. 2011),
increased herbivore populations (“g” in Fig. 2; Hernandez
et al. 2010) and higher grazer diversity (“i”, “f” in Fig. 2;
Hawkins et al. 2009), and – enhanced by eutrophication –
blooms of epiphytes (“h”, “k” in Fig. 2) (Saunders et al.
2010), all of which would promote a decline of large brown
seaweed species.
2.4 Competition
Competition occurs when two organisms require the same
limited resource(s) (exploitation competition) or when one
organism blocks access of other organisms to resources
required by the latter (interference competition) (e.g. Schiel
& Foster 2006). Macroalgae need hard substratum for attach-
ment, nutrients, O
2
, CO
2
(or HCO
3
-
), numerous micronutri-
ents and trace elements for biomass build-up and light as a
source of energy. Densely suspended particles (e.g. plankton,
seston and sediments), but also shading neighbours as well as
epibionts, interfere with a host alga’s access to energy (“3”,
“7” in Fig. 2). Dense epibiosis may also hinder the access of
thallus cells of their host to gases or nutrients (“3” in Fig. 2;
e.g. Wahl et al. 2011). Sediment deposits may reduce the
availability of settlement substratum through inorganic dep-
osition or organic deposition through the crash of plankton
blooms (Berger et al. 2004). Sessile invertebrates compete
with macroalgae for hard substratum. All primary producers,
plankton, epibiotic algae, neighbouring macroalgae poten-
tially compete for dissolved nutrients. The identity of the
competitors differs among seasons, depth and region. The
intensity of the competition depends on the identity and bio-
mass of competitors, the overlap in required resources, the
local availability of these resources and the capacity of the
species in question to store the resources (Schiel & Foster
2006, Wahl et al. 2011, Karez & Chapman 1998). The capac-
ity of many brown macroalgae to store energy and resource
in a chemical form (laminaran, mannitol and the like) allows
them to survive episodes of reduced resource availability
(e.g. light shortage in winter, nutrient shortage in down-
welling phases, etc.) (Lehvo et al. 2001, Rioux et al. 2009).
Anthropogenic changes to the marine environment have
the potential of modifying actual competitive relationships
(HilleRisLambers et al. 2013, Wahl et al. 2011, Harley et al.
2012a): warming may shift competitive interactions by dif-
ferentially affecting the interacting species; eutrophication
![Fig. 1. Global distribution of the major brown macroalgae species treated in this review [after Steneck & Johnson 2013, in: Bertness, M.D. et al. (2014), Marine Community Ecology and Conservation, Sinauer; GBIF and personal observation of the authors].](/figures/fig-1-global-distribution-of-the-major-brown-macroalgae-3and3b8q.webp)
