DISCUSSION
Climatic changes are leading to species redistributions and consequent
impacts on ecosystem function and services are starting to emerge in
some regions (Pecl et al. 2017). In our study system – shallow reefs
within a warming tropical-temperate transition zone where a major
habitat, kelp forests, is declining - we found clear shifts in the
abundance and trophic composition of a fish community. Our results show
overall increases in fish abundance for most trophic groups, including
both tropical and temperate species. Tropical herbivores increased most
dramatically, whereas temperate planktivores were the only trophic guild
that declined, with no corresponding increase in tropical planktivores
observed. Our results here suggest that changes in pathways of energy
flow may be one of the main impacts of climate change for tropicalised
systems, with planktonic inputs becoming less important, while a higher
proportion of algal productivity gets consumed locally by increasingly
abundant herbivores.
Our 17 year study period encompassed the loss of kelp as one of the
dominant foundation species on these tropicalised reefs (Vergés et
al. 2016). We therefore expected to observe declines of temperate fish
species that use kelp as a resource (directly or indirectly) for food,
cover and/ or shelter. However, 22 of the 26 species that changed in
abundance showed an increase in probability of occurrence, and this
included both tropical and temperate species. Overall, this suggests
that tropicalised reefs that have lost kelp can sustain greater fish
biomass than previous kelp-dominated states. These results are
consistent with observed patterns along the latitudinal coast of Eastern
Australia, which show that total fish biomass in shallow reefs is an
order of magnitude higher in warmer subtropical reefs than in higher
latitude reefs which are dominated by kelp (Holland et al. 2020).
What remains to be established is what is fuelling increases in fish
abundance, as well as an increase in diversity in these tropicalised
reefs? One potential explanation is that new ecological niches are
becoming available as foundation species like kelp decline. However, we
found no evidence that tropical fishes increasing in abundance fill
underrepresented niche spaces. Despite a shift from kelp to turf,
neither tropical nor temperate fishes showed a distinct set of traits
that may facilitate success in a shifted environment. For example,
within the herbivore group, tropical fishes that have dramatically
increased over time do not fill a distinct trait space when compared
with temperate herbivores based on their morphometric traits.
Morphometric analysis also did not show any evidence for an increase in
generalist species, a proposed mechanism for successful establishment of
invaders in the more general field of invasion biology.
An alternative explanation for the observed increase in fish biomass is
that the bottom-up resource base in the system has increased. In
particular, as reefs become tropicalised, it is plausible that a higher
proportion of the primary production is consumed and retained within the
local reef system through the observed increases in the abundance of
herbivorous fish. In temperate kelp forests about 80% of kelp
production is exported as detritus (Krumhansl & Scheibling 2012),
whereas in tropical systems, herbivorous fish consume 50-100% of turf
primary production produced in situ (Hay 1991). As fast-growing turf
algae replace canopy forming kelp, the turnover rates of primary
production (time taken to replace biomass) accelerates and the
proportion of primary productivity consumed locally may be increasing,
leading to higher fish biomass (Vergés et al. 2019). Increasing
abundance of herbivorous fish in tropicalised reefs may also lead to
more localised recycling of nutrients, as more local consumption also
means greater supply of nutrients via excretion (Allgeier et al.2017). In turn, this may lead to a higher production of nutritious
detritus, an important food source for many nominal herbivorous fish
(Wilson et al. 2003).
A third possibility for the observed increase in richness and abundance
with no addition of unique niches, also related to the resource base of
the system, is that the fish community studied here is currently well
under the carrying capacity of the system. Thus, despite a phase shift,
increased high fish biomass is still supported making competitive
exclusion currently less important for predicting species change in
occurrence. Perhaps the increasing abundance of range expanding fishes
has a low net effect on the resident community because the loss of
structurally complex kelps has not significantly reduced the carrying
capacity of these reefs, which may have alternative types of
microhabitats and resources. An increase in richness and abundance could
be a combination of both an increase in retained primary productivity
and a fish community at abundance levels not limited by competition.
However, while this may explain an increase in tropical species over the
study period, a cumulative increase in abundance of temperate plus
tropical species is less clear.
It is important to note that many of the species observed increasing in
abundance have cosmopolitan distributions throughout Australia. While
they contribute in our samples to biodiversity enhancement at the local
scale, they may in fact be contributing to broader scale homogenisation
of biodiversity. Scaling up local losses of rare or endemic species
results in a net decrease in regional scale diversity. While in these
tropicalised reefs we found that net gains in species seem to outweigh
net losses, Finderup Nielsen et al. (2019) show that localised increases
in species richness can mask broader patterns of biotic homogenisation
where rare, range-restricted species are almost always disproportionally
the losers. We found evidence of that here with a mix of tropical and
temperate fishes increasing and only temperate species showing a
decline. Although BRUV surveys can underestimate richness and diversity
metrics, roving underwater visual censuses undertaken by divers in the
Solitary Islands during 2001-2017 also reported strong increasing
patterns of species richness for tropicalised mid-shelf reefs (Malcolm
& Ferrari 2019).
The positive correlation between kelp decline and overall fish abundance
and species richness may be reflecting a transitional stage, with
further responses lagging and yet to manifest. For instance, a recent
global synthesis of assemblage changes associated with terrestrial
forest loss has shown that despite evidence for short-term positive
effects on species diversity, there can be lagged responses of up to
decades post tree-loss disturbances, particularly when assemblages
include species with long generation times (Daskalova et al.2020). Similarly, lag effects have been identified in response to
reduced structural complexity following mass bleaching in coral reefs
where, despite initial maintenance of biomass, evidence from size
structure analysis revealed that adult fish lost through natural
mortality are not replaced by juveniles in the long term (Grahamet al. 2007). In a similar way, there may be a time-lag response
to the loss of kelp for long-lived fish species that depend on this
habitat for recruitment or during their juvenile life stages, but are
less dependent on kelp during their adult stages. This fish community is
likely still in transition and longer-term effects of a climate mediated
phase shift may not yet be fully realised. Continued long-term
monitoring of assemblages following disturbances will be key to fully
understand the impacts of habitat change on biodiversity.
Temperate planktivores were the only group that declined over time. The
decline in planktivores observed was largely driven by a decline in the
Australian Mado (Atypichthys strigatus ), an abundant species on
subtropical and temperate rocky reefs in south-eastern Australia. Small
schooling planktivores such as A. strigatus can be considered
outliers in BRUV analyses because they form large groups with highly
stochastic distribution; thus, these results need to be interpreted with
caution. Our results suggest that declines of this broad trophic group
were unlikely due to direct negative competitive interactions with
tropical planktivores, which did not change throughout the study period.
It is interesting to note that an expansion in the distribution ofA. strigatus towards the cold edge of its thermal range and into
Tasmania has been documented (Last et al. 2011). This may suggest
that the decline of this species may be driven by physiological effects
of warming driving a range contraction at the warm edge rather than
shifts in ecological interactions, although complex indirect effects not
quantified here could also explain such declines. Given the dominance
and important role of planktivores in fuelling food webs in shallow
coastal reefs across Australia and New Zealand (Truong et al.2017), a potential range contraction of this species may have important
ecological implications.
In contrast, the decline of the two temperate wrasse species
(Ophthalmolepis lineolatus and Pictilabrus laticlavius )
observed in our study may be directly linked to the decline of kelp, as
these species are known to display a behavioural preference for this
macroalgal habitat (Barrett 1995; Edgar et al. 2004; Tuyaet al. 2009; Fulton et al. 2016). Kelp canopies may be
important for both wrasses through the provision of shelter and refuge
from predation (Tupper & Boutilier 1997); and structurally complex kelp
holdfasts harbour high invertebrate densities that provide a profitable
food source for wrasses (Morton et al. 2008). In the case of the
other species observed declining, the piscivore Dinolestes leweni(Long-fin Pike), we note that this species occupies a relatively unique
niche by the standards of our model, i.e it occupies a large area within
the convex hull and is not clustered towards the mean. This may indicate
niche requirements that are not shared by others in the guild, and may
now no longer be available, e.g. a specialist diet of a declining
species. In their core range, long-fin pike are abundant and feed on
small bodied planktivores including A. strigatus (Truong et
al. 2017).
Shifts in predator-prey interactions due to climate change and species
redistributions are largely unexplored. Here we briefly consider that
the decline of the four temperate species identified in this study could
be partly caused by an overall increase in piscivory, given that ten out
of the 22 species observed increasing in abundance are piscivores with
only one temperate associated piscivore showing a decline. While
in-depth dietary analysis would be required to test this, loss of canopy
cover of kelp may also make some species more vulnerable to predation. A
factor that may have potentially contributed to increased predatory fish
abundance is the establishment of the Solitary Islands Marine Park in
2002. Although none of the study sites are within sanctuary zones where
fishing is totally prohibited, it is possible that increases in predator
abundance are influenced by a spill over effect, i.e. the emigration of
juveniles and/ or adults from protected sanctuary zones to nearby areas.
Most studies find however, that spill over occurs at distances within
200m from no-take zones (Di Lorenzo et al. 2020), and our study
sites were located further away. We therefore consider it unlikely that
fishing regulations are influencing changes in fish abundance in our
study sites, with the notable exception of the observed increases in the
threatened black cod (Epinephelus daemelli ) which are likely to
be a response to targeted management recovery plans for this species
(Harasti & Malcolm 2013).
To summarise, our results suggest that although tropicalisation and
associated loss of kelp can lead to increases in fish diversity and
overall fish abundance, it is also leading to the loss of some temperate
species and is causing major changes in pathways of energy flow, as
reflected by rapid shifts in trophic composition. We hypothesise that
continued warming and tropicalisation will favour range expanding
species and may lead to increases in fish abundance and biomass. Our
data here also suggests that this may be to the detriment of some
temperate associated species. In particular, we observed the decline for
four temperate fishes (Australian mado, southern maori wrasse, senator
wrasse and long fin pike), which may be the first species identified as
vulnerable to changes associated with tropicalisation for this region.
The continued growth of tropical fish populations on high latitude reefs
means that losses of temperate associated fishes may go undetected
particularly if these are not target fisheries species.