Ling SD and Keane JP (2024), Climate-driven invasion and incipient warnings ...

ECB-ART-52743

Nat Commun 2024 Jan 09;151:400. doi: 10.1038/s41467-023-44543-x.

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Climate-driven invasion and incipient warnings of kelp ecosystem collapse.

Ling SD , Keane JP .

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Climate change is progressively redistributing species towards the Earth's poles, indicating widespread potential for ecosystem collapse. Detecting early-warning-signals and enacting adaptation measures is therefore a key imperative for humanity. However, detecting early-warning signals has remained elusive and has focused on exceptionally high-frequency and/ or long-term time-series, which are generally unattainable for most ecosystems that are under-sampled and already impacted by warming. Here, we show that a catastrophic phase-shift in kelp ecosystems, caused by range-extension of an overgrazing sea urchin, also propagates poleward. Critically, we show that incipient spatial-pattern-formations of kelp overgrazing are detectable well-in-advance of collapse along temperate reefs in the ocean warming hotspot of south-eastern Australia. Demonstrating poleward progression of collapse over 15 years, these early-warning 'incipient barrens' are now widespread along 500 km of coast with projections indicating that half of all kelp beds within this range-extension region will collapse by ~2030. Overgrazing was positively associated with deep boulder-reefs, yet negatively associated with predatory lobsters and subordinate abalone competitors, which have both been intensively fished. Climate-driven collapse of ecosystems is occurring; however, by looking equatorward, space-for-time substitutions can enable practical detection of early-warning spatial-pattern-formations, allowing local climate adaptation measures to be enacted in advance.

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	Fig. 1. Southeast Australian study system showing coastal warming, climate-driven invasion by the Longspined sea urchin, and spatial pattern formation of ecosystem collapse.a Heatmap showing Sea Surface Temperature influence of the warm East Australian Current (EAC), which extends southward from New South Wales (NSW) to Tasmania where 13 east coast reef sites (listed 1–13 from north to south) were surveyed in 2001/02 and 2016/17 (map created in Matlab R2023a); years along the coast indicate the progressive poleward timeline of first occurrences of the sea urchin extending its range from NSW (SST data are means for August 2008–2018; IMOS multi-sensor SST composites: http://rs-data1-mel.csiro.au/thredds/catalog/imos-srs/sst/ghrsst/L3S-1d/catalog.html). Inset plot in a shows size-distribution of barrens patches (semi-transparent points plotted log-scale on x axis ranging 1, to 1 thousand, to 1 million m2), with progressively smaller barrens occurring southward along the invasion-front as estimated in situ by divers for a total of 1297 barrens patches during 2008 to 2011; source data are provided as a Source Data file. b Long-term August (winter) sea temperature trend (1944–2017) from the Maria Island oceanographic station (Site 7): https://portal.aodn.org.au/); August is the month of spawning for the sea urchin C. rodgersii, with larvae (inset image) only developing above 12 °C (dashed horizontal line15), timing of surveys are shown as upward arrows on x axis (2001/02 = blue; 2016/17 = red); inset images taken in 2018 at Maria Island (Site 7, kelp) and St. Helens (Site 2, barrens). c Schematic of the spatial pattern of ecosystem collapse from kelp forests to urchin barrens via intermediate ‘incipient barrens’, which expand and coalesce as urchin density increases across reefs. d Schematic of observed climate-driven spatial pattern formation in the poleward direction; following from bottom-to-top provides a space-for-time substitution of the process of collapse from kelp to extensive barrens via appearance and ultimately coalescence of incipient barrens as the overgrazing tipping-point in urchin density is increasingly exceeded.
	Fig. 2. Space-time dynamics of urchin invasion and catastrophic phase-shift from kelp to barrens.Box plots of a C. rodgersii abundance, and b barrens coverage by period (blue = 2001–02; red = 2016–17) as assessed by divers, sites numbered north to south along coast (n = 3 subsites per site, with 4 transects within each subsite); box plots show median (50th percentile) as a horizontal bar, with upper and lower bounds of box defined as the 75th and 25th percentiles, whiskers extend to 1.5 times this interquartile range, outliers are shown as individual points occurring beyond >1.5 times interquartile range. c phase-shift dynamics between total kelp cover and C. rodgersii density through time as measured at 5 m2 quadrat scale. Source data are provided as a Source Data file. c downward and upward dashed-arrows indicate tipping-points of overgrazing (i.e., ~2.2 urchins.m−2) and kelp recovery (i.e., ~0.36 individ.m−2)17; solid lines are simplified mean trendlines fitted to all data in 2001/02 (blue), y = −19.82x + 100.31, R2 = 0.56, n = 1600 quadrats; and 2016/17 (red), y = −33.58x + 99.85, R2 = 0.65, n = 1600 quadrats (red downward arrow indicates collapse of kelp through time); histogram on right of panel projects the frequency distribution of quadrats within 20% bins of kelp cover, showing increasing bimodality between high cover kelp beds and collapsed urchin barrens through time, 2001/02 (blue) to 2016/17 (red).
	Fig. 3. Urchin invasion dynamics and overgrazed barrens by depth and reef type in eastern Tasmania.Change in C. rodgersii abundance (a–c), and barrens cover (d–f) by substratum type and depth category (4–18 m depth) pooled for sites 1–9 in each period, box plots as per Fig. 2. Data are densities derived from 5 m2 quadrats assessed by divers and averaged for quadrats dominated (>50% cover) by a particular substratum type within 2 m depth categories, depths shown represent the ceilings of each category; n quadrats within each category for both urchin abundance (a–c) and barrens cover (d–f) are shown in parentheses above boxes in (a–c) with each period separated by comma. Source data are provided as a Source Data file.
	Fig. 4. Propagation of collapse from incipient to continuous barrens.Incipient barrens of small [0.2−2 m diam.] (a), medium [2–4 m diam.] (b), and large [4–8.5 m diam.] (c) patch-sizes increased dramatically from 2001/02 (blue) to 2016/17 (red) indicating pending broadscale collapse to continuous barrens (d), with overall planar cover of barrens (e) also increasing markedly; the effect of “Time” was significant for all barrens response variables across eastern Tasmania, see Supplementary Table 5; box plots as per Fig. 2, with values at the site level generated from means of n = 4 video-tows ranging 4–40 m depth at n = 3 subsites. For incipient barrens (a) and planar sum of barrens (e), pre-planned one-tailed comparison of increase in percentage cover within each site is indicated by the significance codes: ‘’ <0.01, ‘*’ <0.001. Source data are provided as a Source Data file.

References [+] :

Gervais, Species on the move around the Australian coastline: A continental-scale review of climate-driven species redistribution in marine systems. 2021, Pubmed