The Dynamic Biogeography of the Anthropocene: The Speed of Recent Range Shifts in Seaweeds

Abstract

The biogeographic boundaries of seaweeds are largely determined by temperature tolerances, physical barriers and limitations to dispersal. Anthropogenic ocean warming and increasing connectivity through human activities are now causing rapid changes in the biogeography of seaweeds. Globally, at least 346 non-native seaweed taxa have been introduced to new regions, and at least 31 species of seaweed have shifted their distributions in response to recent temperature changes. Range-shift speeds were determined for 40 taxa, and compared between three drivers: (I) range expansions caused by introductions, (II) range expansions and (III) contractions caused by climate change (warming/cooling). The speed of change in seaweed biogeography differed between these drivers of change, with expansions significantly faster than contractions, and climate-driven shifts significantly slower than introductions. Some of the best documented introduced species expansions include Sargassum muticum (4.4 km/year in Denmark), Undaria pinnatifida (35–50 km/year in Argentina) and Caulerpa cylindracea (11.9 km/year in the Mediterranean Sea). Examples of seaweeds with recent climate-driven range shifts include Scytothalia dorycarpa, a native species in Western Australia, which retracted >100 km poleward as a consequence of a single event (a regional marine heat wave). However, climate-driven range shifts were generally assessed over long time periods (>10 years). Fucus serratus (1.7 km/year) and Himanthalia elongata (4.4 km/year) have slowly retracted westwards in northern Spain in response to warming in the Bay of Biscay. In England and South Africa, Laminaria ochroleuca (5.4 km/year) and Ecklonia maxima (36.5 km/year) have expanded their ranges in response to local warming and cooling, respectively. These changes in seaweed biogeography likely have had substantial implications for biodiversity and ecosystem processes, particularly where the shifting seaweeds have been canopy-forming foundation species. We discuss some of these consequences and different attributes of climate and invasion-driven range shifts in seaweeds.

Appendix

Review of published literature and citation searches to compile a global dataset of documented range shifts in native seaweeds or range expansions of successful seaweed invaders. Used key words include climate change , warming, extreme events , heat waves, invasive seaweeds , successful invaders, shift in distribution, range shifts , range expansion and range contraction . Literature was included when data was available for the direction, distance and time window of seaweed shift, so annual spread rates could be calculated. Literature stating a decrease in abundance or not pinpointing location and time window were excluded from the dataset. The two main drivers are Introduction (introduction) and Warming (contraction/expansion). When unusual driver it is added in brackets

Species	Division	Region	Driver	Annual spread (km/years)	First appearance/absence	Time window (years)	Distance (km)	Reference
Assemblage	Assemblage	SW Australia	Contraction	1.0	1940	50	51	Wernberg et al. (2011a, b)
Assemblage	Assemblage	SE Australia	Contraction	4.2	1940	50	211	Wernberg et al. (2011a, b)
Caulerpa cylindracea	Chlorophyta	Provence, France	Introduction	11.9	1997	7	83	Ruitton et al. (2005)
Caulerpa cylindracea	Chlorophyta	Ligurian Sea	Introduction	44.0	2009	5	220	Altamirano et al. (2014)
Caulerpa ollivieri	Chlorophyta	Mexico	Introduction	19.0	1968	42	800	Ortegón-Aznar et al. (2015)
Caulerpa taxifolia var. distichophylla	Chlorophyta	Mediterranean Sea	Introduction	33.3	2006	6	200	Aplikioti et al. (2016)
Caulerpa taxifolia var. distichophylla	Chlorophyta	Mediterranean Sea	Introduction	87.5	2006	8	700	Aplikioti et al. (2016)
Codium adhaerens	Chlorophyta	Portugal	Expansion	1.2	1955	50	59	Lima et al. (2007)
Codium fragile ssp. fragile	Chlorophyta	Nova Scotia	Introduction	11.1	1989	18	200	Watanabe et al. (2010)
Codium fragile ssp. tomentosoides	Chlorophyta	NW Atlantic	Introduction	16.0	1955	47	750	Scheibling and Gagnon (2006)
Codium fragile ssp. tomentosoides	Chlorophyta	NW Atlantic	Introduction	10.6	1955	47	500	Scheibling and Gagnon (2006)
Codium fragile ssp. tomentosoides	Chlorophyta	Northern Chile	Introduction	6.4	2005	7	45	Neill et al. (2006)
Valonia utricularis	Chlorophyta	Portugal	Expansion	3.9	1955	50	197	Lima et al. (2007)
Ahnfeltia plicata	Ochrophyta	Portugal	Expansion	6.6	1955	50	330	Lima et al. (2007)
Bifurcaria bifurcata	Ochrophyta	Britain, Ireland	Expansion	3.1	1964	45	140	Mieszkowska et al. (2006)
Bifurcaria bifurcata	Ochrophyta	Portugal	Expansion	5.1	1955	50	257	Lima et al. (2007)
Chondrus crispus	Ochrophyta	Portugal	Expansion	3.6	1955	50	180	Lima et al. (2007)
Desmarestia aculeata	Ochrophyta	Portugal	Expansion	4.5	1955	50	227	Lima et al. (2007)
Desmarestia ligulata	Ochrophyta	Portugal	Expansion	1.4	1955	50	70	Lima et al. (2007)
Dumontia contorta	Ochrophyta	Portugal	Expansion	1.2	1955	50	62	Lima et al. (2007)
Durvillea potatorum	Ochrophyta	SE Australia	Contraction	0.6	1945	60	35	Millar (2007)
Ecklonia maxima	Ochrophyta	South Africa	Expansion	36.5	2008	2	73	Bolton et al. (2012)
Ecklonia radiata	Ochrophyta	SW Australia	Contraction	88.0	2011	1	88	Wernberg and Bennett, unpublished data 2015
Fucus serratus	Ochrophyta	North Spain	Contraction	1.9	1894	60	116	Duarte et al. (2013)
Fucus serratus	Ochrophyta	North Spain	Contraction	5.1	1955	21	107	Duarte et al. (2013)
Fucus serratus	Ochrophyta	North Spain	Expansion	2.2	1977	12	26	Duarte et al. (2013)
Fucus serratus	Ochrophyta	Spain	Expansion	5.0	1982	20	100	Arrontes (2002)
Fucus serratus	Ochrophyta	North America	Introduction	11.8	1868	17	200	Johnson et al. (2012)
Fucus serratus	Ochrophyta	North America	Introduction	5.3	1868	17	90	Johnson et al. (2012)
Fucus vesiculosus	Ochrophyta	Morocco	Contraction	41.7	1985	30	1250	Nicastro et al. (2013)
Fucus vesiculosus	Ochrophyta	Portugal	Expansion	3.1	1955	50	157	Lima et al. (2007)
Halidrys siliquosa	Ochrophyta	Portugal	Expansion	1.8	1955	50	90	Lima et al. (2007)
Halydris siliquosa	Ochrophyta	Portugal	Expansion	1.1	2006	75	80	Lima et al. (2008)
Himanthalia elongata	Ochrophyta	North Spain	Contraction	1.8	1889	66	116	Duarte et al. (2013)
Himanthalia elongata	Ochrophyta	North Spain	Contraction	4.2	1955	20	84	Duarte et al. (2013)
Himanthalia elongata	Ochrophyta	North Spain	Contraction	26.0	2004	5	130	Duarte et al. (2013)
Himanthalia elongata	Ochrophyta	Portugal	Expansion	4.4	1955	50	219	Lima et al. (2007)
Laminaria ochroleuca	Ochrophyta	SE Atlantic	Expansion	2.5	1948	60	150	Smale et a (2013)
Laminaria ochroleuca	Ochrophyta	SE Atlantic	Expansion	5.4	1948	60	325	Smale et al. (2013)
Padina pavonica	Ochrophyta	Portugal	Expansion	3.7	1955	50	187	Lima et al. (2007)
Pelvetia canaliculata	Ochrophyta	Portugal	Expansion	4.9	1955	50	245	Lima et al. (2007)
Sargassum filicinum	Ochrophyta	Mexico	Introduction	137.5	2003	4	550	Riosmena-Rodriguez (2012)
Sargassum flavifolium	Ochrophyta	Portugal	Expansion	11.9	1955	50	593	Lima et al. (2007)
Sargassum illicifolium	Ochrophyta	Japan	Expansion	10.5	1989	19	200	Tanaka et al. (2012)
Sargassum micracanthum	Ochrophyta	Japan	Contraction	3.9	1977	31	120	Tanaka et al. (2012)
Sargassum muticum	Ochrophyta	Denmark	Introduction	4.4	1984	16	70	Staehr et al. (2000)
Sargassum muticum	Ochrophyta	Canada	Introduction	111.2	1947	6	667	Engelen et al. (2015)
Sargassum muticum	Ochrophyta	northern California	Introduction	80.6	1965	18	1450	Engelen et al. (2015)
Sargassum muticum	Ochrophyta	Mexico	Introduction	35.0	1973	8	280	Engelen et al. (2015)
Sargassum muticum	Ochrophyta	Netherlands	Introduction	50.0	1979	6	300	Engelen et al. (2015)
Sargassum muticum	Ochrophyta	Denmark	Introduction	120.0	1984	5	600	Engelen et al. (2015)
Sargassum muticum	Ochrophyta	France	Introduction	81.8	1983	11	900	Engelen et al. (2015)
Sargassum muticum	Ochrophyta	Mexico	Introduction	2.7	1988	15	40	Espinoza (1990)
Sargassum yamamotoi	Ochrophyta	Japan	Contraction	4.4	1977	31	135	Tanaka et al. (2012)
Scytothalia dorycarpa	Ochrophyta	SW Australia	Contraction	100.0	2011	1	100	Smale and Wernberg (2013)
Scytothalia dorycarpa	Ochrophyta	SW Australia	Contraction	3.2	1961	50	160	Smale and Wernberg (2013)
Turbinaria ornata	Ochrophyta	French Polynesia	Expansion	30.0	1980	10	300	Stewart (2008)
Undaria pinnatifida	Ochrophyta	North America	Introduction	125.0	2000	2	250	Aguilar-Rosas et al. (2004)
Undaria pinnatifida	Ochrophyta	Mexico	Introduction	66.7	2003	3	200	Aguilar-Rosas et al. (2004)
Undaria pinnatifida	Ochrophyta	Argentina	Introduction	35.7	1999	7	250	Dellatorre et al. (2014)
Undaria pinnatifida	Ochrophyta	Argentina	Introduction	50.0	2005	6	300	Dellatorre et al. (2014)
Undaria pinnatifida	Ochrophyta	Argentina	Introduction	50.0	2012	20	1000	Dellatorre et al. (2014)
Grateloupia doryphora	Rhodophyta	Brittany, France	Introduction	150.0	1999	1	150	Simon et al. (2001)
Grateloupia turuturu	Rhodophyta	Gulf of Maine	Introduction	33.0	2007	4	132	Mathieson et al. (2008)
Halopithys incurva	Rhodophyta	Portugal	Expansion	9.5	1955	50	475	Lima et al. (2007)
Heterosiphonia japonica	Rhodophyta	Western North Atlantic	Introduction	66.7	2007	6	400	Newton et al. (2013)
Heterosiphonia japonica	Rhodophyta	Western North Atlantic	Introduction	16.7	2007	6	100	Newton et al. (2013)
Hypnea musciformis	Rhodophyta	Portugal	Expansion	5.4	1955	50	269	Lima et al. (2007)
Mastocarpus sp.	Rhodophyta	Chile	Introduction	18.2	1980	22	400	Macaya et al. (2013)
Mastocarpus sp.	Rhodophyta	Chile	Introduction	31.8	1980	22	700	Macaya et al. (2013)
Palmaria palmata	Rhodophyta	Portugal	Expansion	7.2	1955	50	358	Lima et al. (2007)