Introduction
Competitive interactions among primary producers have been widely shown
to shift to facilitative when conditions become stressful, as predicted
by the Stress Gradient Hypothesis (SGH; Bertness & Callaway 1994; Bruno
et al. 2003; He et al. 2013). For example, in a study of alpine plant
interactions, identically and globally replicated experiments
demonstrated that interactions shifted from competitive at low
elevations to facilitative at higher, more stressful, elevations
(Callaway et al. 2002). This shift from competitive to facilitative
interactions along gradients of stress has likewise been shown for arid
plants and nurse shrubs (Armas et al. 2011), pitcher plants and spiders
(Lim et al. 2018), and alpine herbivores (Barrio et al. 2013), among
others. Similar to terrestrial elevational shifts from negative to
positive interactions, species interactions among marine and limnal taxa
have also been shown to shift from competitive to facilitative in 1)
drier, more stressful tidal elevations (intertidal marsh plants:
Bertness & Hacker 1994; barnacles and mussels: Kawai & Tokeshi 2007),
and in 2) warmer, more stressful latitudes (Bennett et al. 2015; McAfee
et al. 2016). Despite being well-documented in terrestrial and brackish
ecosystems, the SGH has not been tested in marine forests, and instead
competition is thought to be the dominant structuring mechanism (though
see Bennett et al. 2015). In this study, marine forest ecosystems were
used to examine influences of species facilitation, positive
interactions and principles of the SGH in structuring algal communities.
The past decade has seen dramatic declines in marine forest cover (Ling
et al. 2015; Krumhansl et al. 2016; Wernberg et al. 2016; Vergés et al.
2016). Foundation species provide habitat and energy to associated
organisms (Dayton 1972), ultimately increasing biodiversity. Foundation
species persistence is critical for understanding the dynamics of the
systems they sustain. One of the most well studied, conspicuous groups
of foundation species are canopy-forming brown seaweeds, belonging
primarily to the orders Laminariales (kelp) and Fucales (fucoids). Many
disturbed marine forests are shifting from canopy-dominated to systems
dominated by turf-forming or crustose algae (Filbee-Dexter & Scheibling
2014; Filbee-Dexter & Wernberg 2018), an example of alternative stable
states (Dayton & Tegner 1984). With a suite of abiotic and biotic
stressors contributing to the decline of kelp forests, their recovery is
thought to be prevented, in part, by competition with algal species that
live in the understory (Filbee-Dexter & Scheibling 2014; Filbee-Dexter
& Wernberg 2018).
Negative effects of algal turfs on canopies are well supported from
long-term subtidal research programs and experimental studies (Dayton et
al. 1984; Hernández -Carmona et al. 2005; Gorman & Connell 2009).
Although many canopy-forming species are dominant competitors (Dayton et
al. 1984), abiotic and biotic disturbance can lead to the dominance of
turf algae, if those turf algae compete with the canopy (Fig. 1A). For
example, the co-occurrence of El Niño-driven warm temperatures, nutrient
depletion, and unusually strong storms devastated more than 500 hectares
of kelp forest in southern California (Dayton & Tegner 1984). In the
wake of massive loss of kelp adults and kelp recruitment failure, a new,
turf-dominated community emerged, comprised of turf species and
subdominant understory kelp. Algal turfs, unaffected by the El Niño
disturbances, inhibited the recruitment of new canopy kelp, slowing the
kelp forest recovery (Dayton et al. 1984). Although the kelp forest
generally recovered after this El Niño, the kelp-dominated community
never returned at its southernmost range edge (Hernández-Carmona et al.
2005). The dominance of these turf species, particularly
herbivore-resistant coralline algae, is often maintained by the presence
of kelp grazers (Vergés et al. 2016), forming the classic coralline
algae/urchin barren alternative stable state (Filbee-Dexter &
Scheibling 2014). The assumption of competitive exclusion by the turf
now forms the basis of recommended restoration practices
(Hernandez-Carmona et al. 2005) and even predictions for the future of
canopy-forming marine ecosystems (Connell et al. 2013). For example, in
the turf-as-competitors framework (Fig. 1A), as coralline turfs are
expected to decline with ocean acidification, kelp abundance would be
expected to increase under ocean acidification, due to the assumed
release from competition and physiological effects from increasedp CO2 (Harley et al. 2012). Despite the dominance
of the competition framework in the study of marine forests, many
examples exist of canopy facilitation by turfs (Fig. 1B). These examples
of facilitation have yet to be comprehensively incorporated into our
understanding of canopy-turf dynamics or marine forest alternative
stable states.
In this study, we approach competition and facilitation in marine
forests within the framework of the SGH and the well-documented patterns
seen in terrestrial systems. We examine the longstanding hypothesis that
the effect of turf algae on canopy-forming species is competitive, using
a new global dataset of marine turf-canopy interactions. We used
meta-analysis to answer the following questions: a) What is the overall
effect of the turf on canopy-forming seaweeds? b) Does this effect
differ among turf functional groups? c) Does the effect of turfs on the
canopy vary along stress gradients, i.e. depth? d) Does the effect of
turfs on the canopy vary latitudinally?, and d) Does herbivory modify
the effect of turfs on the canopy? We expand the number of studies
previously included in a meta-analysis of kelp-turf interactions
four-fold, and broaden the scope from the effect only on recruitment to
the effect on all life-history stages of canopy forming species (O’Brien
& Scheibling 2018). We show that the previously well-documented
competitive effects of turf species on canopy species are part of a
continuum of positive to negative interactions that depend predictably
on stress.