Editing IPCC:AR6/SROCC/Chapter-5 (section)

===== 5.2.3.1.1 Detection and attribution of biological changes in the epipelagic ocean Temperature-driven shifts in distribution and phenology =====

WGII AR5 concluded that the vulnerability of most organisms to warming is set by their physiology, which defines their limited temperature ranges and thermal sensitivity (Pörtner et al., 2014 <sup>[[#fn:r385|385]]</sup> ). Although different hypotheses have been proposed since AR5 to explain the mechanism linking temperature sensitivity of marine organisms and their physiological tolerances (Schulte, 2015 <sup>[[#fn:r386|386]]</sup> ; Pörtner et al., 2017 <sup>[[#fn:r387|387]]</sup> ; Somero et al., 2017 <sup>[[#fn:r388|388]]</sup> ), evidence from physiological experiments and observations from paleo- and contemporary periods continue to support the conclusion from AR5 on the impacts of temperature change beyond thermal tolerance ranges on biological functions such as metabolism, growth and reproduction (Payne et al., 2016 <sup>[[#fn:r389|389]]</sup> ; Pörtner and Gutt, 2016 <sup>[[#fn:r390|390]]</sup> ; Gunderson et al., 2017 <sup>[[#fn:r391|391]]</sup> ), contributing to changes in biogeography and community structure (Beaugrand et al., 2015 <sup>[[#fn:r392|392]]</sup> ; Stuart-Smith et al., 2015 <sup>[[#fn:r393|393]]</sup> ) ( ''high agreement, high confidence'' ). Comparison of biota across land and ocean suggests that marine species are generally inhabiting environment that is closer to their upper temperature limits, explaining the substantially higher rate of local extirpation related to warming relative to those on land (Pinsky et al., 2019 <sup>[[#fn:r394|394]]</sup> ). Hypoxia and acidification can also limit the temperature ranges of organisms and exacerbate their sensitivity to warming (Mackenzie et al., 2014 <sup>[[#fn:r395|395]]</sup> ; Rosas-Navarro et al., 2016 <sup>[[#fn:r396|396]]</sup> ; Pörtner et al., 2017 <sup>[[#fn:r397|397]]</sup> ), although interactions vary strongly between species and biological processes (Gobler and Baumann, 2016 <sup>[[#fn:r398|398]]</sup> ; Lefevre, 2016 <sup>[[#fn:r399|399]]</sup> ).

Shifts in distribution of marine species from phytoplankton to marine mammals continued to be observed since AR5 across all ocean regions (Poloczanska et al., 2016 <sup>[[#fn:r400|400]]</sup> ). Recent evidence continues to support that a large proportion of records of observed range shifts in the epipelagic ecosystem (Poloczanska et al., 2016 <sup>[[#fn:r401|401]]</sup> ) are correlated with ocean temperature, with an estimated average shift in distribution (including range centroids, northward and southward boundaries) from these records of 51.5 ± 33.3 km per decade since the 1950s (Figure 5.13). Such rate of shift is significantly faster than those records for organisms in the seafloor; the latter has an average rate of distribution shift of 29.0 ± 15.5 km per decade (44% of the records for seafloor species with range shifts that are consistent with expectation from the observed temperature changes)( ''very likely'' ) (Figure 5.13). Comparison of global seafloor-derived planktonic foraminifera from pre-industrial age with recent (from year 1978) communities show that the recent assemblages differ from their pre-industrial with increasing dominance of warmer or cooler species that are mostly consistent with temperature changes (Jonkers et al., 2019 <sup>[[#fn:r402|402]]</sup> ). Rate of observed responses also varies between and within animal groups among ocean regions, with zooplankton and fishes having faster recorded range shifts (Pinsky et al., 2013 <sup>[[#fn:r403|403]]</sup> ; Asch, 2015 <sup>[[#fn:r404|404]]</sup> ; Jones and Cheung, 2015 <sup>[[#fn:r405|405]]</sup> ; Poloczanska et al., 2016 <sup>[[#fn:r406|406]]</sup> ). For example, analysis of the Continuous Plankton Recorder (CPR) data-series from the north Atlantic in the last decades shows that the range of dinoflagellates tended to closely track the velocity of climate change (the rate of isotherm movement). In contrast, the distribution range of diatoms shifted much more slowly (Chivers et al., 2017 <sup>[[#fn:r407|407]]</sup> ) and its distribution seems to be primary influenced by multi-decadal variability rather than from secular temperature trends. The CPR surveys have also provided evidence that some calanoid copepods are expanding poleward in the Northeast Atlantic, at a rate up to 232 km per decade (Beaugrand, 2009 <sup>[[#fn:r408|408]]</sup> ; Chivers et al., 2017 <sup>[[#fn:r409|409]]</sup> ), although different calanoid species respond differently in the rate and direction of shifts (Philippart et al., 2003 <sup>[[#fn:r410|410]]</sup> ; Edwards and Richardson, 2004 <sup>[[#fn:r411|411]]</sup> ; Asch, 2015 <sup>[[#fn:r412|412]]</sup> ; Crespo et al., 2017 <sup>[[#fn:r413|413]]</sup> ). Overall, the observed changes in biogeography are consistent with expected responses to changes in ocean temperature for the majority of marine biota ( ''high confidence'' ). This is also consistent with theories and experimental evidence that scale from individual organisms’ physiological responses to community level effects ( ''high confidence'' ). Sensitivity of organisms’ biogeography varies between taxonomic groups ( ''high confidence'' ).

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'''Figure 5.13'''

<span id="figure-5.13-evidence-of-climate-change-responses-of-marine-organisms-to-changes-in-ocean-conditions-under-climate-change.-a-evidence-of-interactive-effects-including-synergistic-and-antagonistic-of-multiple-climatic-hazards-based-on-przeslawski-et-al.-2015-lefevre-2016-section-5.2.2-5.2.3-5.2.4-5.3.-others-mainly-include-mammals-seabirds-and-marine-reptiles.-the-lighter-coloured"></span>
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'''Figure 5.13 | Evidence of climate change responses of marine organisms to changes in ocean conditions under climate change. (a) evidence of interactive effects (including synergistic and antagonistic) of multiple climatic hazards (based on Przeslawski et al. (2015); Lefevre (2016); Section 5.2.2, 5.2.3, 5.2.4, 5.3). ‘Others’ mainly include mammals, seabirds and marine reptiles). The lighter-coloured […]'''
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Figure 5.13 | Evidence of climate change responses of marine organisms to changes in ocean conditions under climate change. (a) evidence of interactive effects (including synergistic and antagonistic) of multiple climatic hazards (based on Przeslawski et al. (2015); Lefevre (2016); Section 5.2.2, 5.2.3, 5.2.4, 5.3). ‘Others’ mainly include mammals, seabirds and marine reptiles). The lighter-coloured cell represents insufficient information to draw conclusion; (b–d) observations on changes in latitudinal range and (e–h) phenology (based on Poloczanska et al. 2013). For b–h, each bar represents one record.

The rate and direction of observed range shifts are shaped by the interaction between climatic and non-climatic factors (Poloczanska et al., 2013 <sup>[[#fn:r414|414]]</sup> ; Sydeman et al., 2015 <sup>[[#fn:r415|415]]</sup> ; Poloczanska et al., 2016 <sup>[[#fn:r416|416]]</sup> ), such as local temperature and oxygen gradients in the habitat across depth (Cheung et al., 2013 <sup>[[#fn:r417|417]]</sup> ; Deutsch et al., 2015 <sup>[[#fn:r418|418]]</sup> ), latitude and longitude (Burrows et al., 2014 <sup>[[#fn:r419|419]]</sup> ; Barton et al., 2016 <sup>[[#fn:r420|420]]</sup> ), ocean currents (Sunday et al., 2015 <sup>[[#fn:r421|421]]</sup> ; Barton et al., 2016 <sup>[[#fn:r422|422]]</sup> ; García Molinos et al., 2017 <sup>[[#fn:r423|423]]</sup> ), bathymetry in all or part of their life stages (for organisms living on or close to the seafloor) (Pinsky et al., 2013 <sup>[[#fn:r424|424]]</sup> ; Kleisner et al., 2015 <sup>[[#fn:r425|425]]</sup> ), geographical barriers (Pinsky et al., 2013 <sup>[[#fn:r426|426]]</sup> ; Burrows et al., 2014 <sup>[[#fn:r427|427]]</sup> ), availability of food and critical habitat (Sydeman et al., 2015 <sup>[[#fn:r428|428]]</sup> ), fishing and other non-climatic human impacts (Engelhard et al., 2014 <sup>[[#fn:r429|429]]</sup> ; Hoegh-Guldberg et al., 2014 <sup>[[#fn:r430|430]]</sup> ). Moreover, observed range shifts in respond to climate change in some regions such as the north Atlantic are strongly influenced by warming due to multi-decadal variability (Edwards et al., 2013 <sup>[[#fn:r431|431]]</sup> ; Harris et al., 2014 <sup>[[#fn:r432|432]]</sup> ), suggesting that there is a longer time-of-emergence of range shifts from natural variability and a need for longer biological time series for robust attribution. The rate of shifts in biogeography of organism is influenced by multiple climatic and non-climatic factors ( ''high confidence'' ) that can result in non-synchronous shifts in community composition ( ''high confidence'' ). There is general under-representation of biogeographical records in low latitudes (Dornelas et al., 2018 <sup>[[#fn:r433|433]]</sup> ), rendering detection and attribution of shifts in biogeography in these regions having ''medium confidence'' . The variation in responses of marine biota to range shifts can cause spatial restructuring of the pelagic ecosystem with consequences for organisms at higher trophic levels (Chivers et al., 2017 <sup>[[#fn:r434|434]]</sup> ; Pecl et al., 2017 <sup>[[#fn:r435|435]]</sup> ) ( ''high confidence'' ). Marine ectotherms have demonstrated some capacity for physiological adjustment and evolutionary adaptation that lowers their sensitivity to warming and decrease in oxygen (Pörtner et al., 2014 <sup>[[#fn:r436|436]]</sup> ; Cavallo et al., 2015 <sup>[[#fn:r437|437]]</sup> ) ( ''low confidence'' ). However, historical responses in abundance and ranges of marine species to ocean warming suggest that adaptation not always suffices to mitigate projected impacts (WGII AR5 Chapter 6) ( ''high confidence'' ).

Marine reptiles, seabirds and mammals breathe air, instead of obtaining oxygen from water, and many of them spend some of their life cycle on land, being their abundance and distribution still affected by temperature (Pörtner et al., 2014 <sup>[[#fn:r438|438]]</sup> ). Long term population changes and shifts in distribution associated with climate change have been observed for temperate species of seabirds and marine mammals (Henderson et al., 2014 <sup>[[#fn:r439|439]]</sup> ; Hiscock and Chilvers, 2014 <sup>[[#fn:r440|440]]</sup> ; Ramp et al., 2015 <sup>[[#fn:r441|441]]</sup> ) ( ''high confidence'' ). For example, Laysan, ''Phoebastria immutabilis,'' and Wandering, ''Diomedea exulans'' , albatross have responded positively to climate change as they have been able to take advantage of the increased intensity of winds. This has allowed them to forage farther and faster, making their foraging trips shorter, increasing their foraging efficiency and breeding success (Descamps et al., 2015 <sup>[[#fn:r442|442]]</sup> ; Thorne et al., 2016 <sup>[[#fn:r443|443]]</sup> ). For reptiles, like sea turtles and snakes, temperature directly affects important life history traits including hatchling size, sex, viability and performance ''(high confidence)'' (Hays et al., 2003 <sup>[[#fn:r444|444]]</sup> ; Pike, 2014 <sup>[[#fn:r445|445]]</sup> ; Dudley et al., 2016 <sup>[[#fn:r446|446]]</sup> ; Santos et al., 2017 <sup>[[#fn:r447|447]]</sup> ). This is particularly important for marine turtles as changing temperatures will affect the hatchling sex ratio because sex is determined by nest site temperature ''(high confidence'' ) (Hatfield et al., 2012 <sup>[[#fn:r448|448]]</sup> ; Santidrián Tomillo et al., 2014 <sup>[[#fn:r449|449]]</sup> ; Patricio et al., 2017 <sup>[[#fn:r450|450]]</sup> ). Loss of breeding substrate, including mostly coastal habitats such as sandy beaches (Section 5.3.3), can reduce the available nesting or pupping habitat for land breeding marine turtles, lizards, seabirds and pinnipeds (Fish et al., 2005 <sup>[[#fn:r451|451]]</sup> ; Fuentes et al., 2010 <sup>[[#fn:r452|452]]</sup> ; Funayama et al., 2013 <sup>[[#fn:r453|453]]</sup> ; Reece et al., 2013 <sup>[[#fn:r454|454]]</sup> ; Katselidis et al., 2014 <sup>[[#fn:r455|455]]</sup> ; Patino-Martinez et al., 2014 <sup>[[#fn:r456|456]]</sup> ; Pike et al., 2015 <sup>[[#fn:r|]]</sup> ; Reynolds et al., 2015; Marshall et al., 2017) ( ''high confidence'' ). Climatic hazards such as SLR contributes to the loss of these coastal habitats (see Section 5.3 and Chapter 3). Changes in ocean temperature will also indirectly impact marine mammals, seabirds and reptiles by changing the abundance and distribution of their prey (Polovina, 2005 <sup>[[#fn:r479|479]]</sup> ; Polovina et al., 2011 <sup>[[#fn:r480|480]]</sup> ; Doney et al., 2012 <sup>[[#fn:r481|481]]</sup> ; Sydeman et al., 2015 <sup>[[#fn:r482|482]]</sup> ; Briscoe et al., 2017 <sup>[[#fn:r483|483]]</sup> ; Woodworth-Jefcoats et al., 2017 <sup>[[#fn:r484|484]]</sup> ) ( ''high confidence'' ). The distributions of some of these large animals is determined by the occurrence and persistence of oceanic bridges and barriers that are related to climate driven processes (Ascani et al., 2016 <sup>[[#fn:r485|485]]</sup> ; McKeon et al., 2016 <sup>[[#fn:r486|486]]</sup> ). For example, the decline of Arctic sea ice is affecting the range and migration patterns of some species and is allowing the exchange of species previously restricted to either the Pacific or Atlantic oceans (Alter et al., 2015 <sup>[[#fn:r487|487]]</sup> ; George et al., 2015 <sup>[[#fn:r488|488]]</sup> ; Laidre et al., 2015 <sup>[[#fn:r489|489]]</sup> ; MacIntyre et al., 2015 <sup>[[#fn:r490|490]]</sup> ; McKeon et al., 2016 <sup>[[#fn:r491|491]]</sup> ; Breed et al., 2017 <sup>[[#fn:r492|492]]</sup> ; Hauser et al., 2017 <sup>[[#fn:r493|493]]</sup> ) (Chapter 3). Also, the range expansion of some of these predatory megafauna can affect species endemic to the habitat; for example, while the decrease in summer sea ice in the Arctic may favour the expansion of killer whales ( ''Orcinus orca'' ), their occurrence can result in narwhale ( ''Monodon monoceros'' ) to avoid the use of key habitats to reduce the risk of killer whales’ predation (Bost et al., 2009 <sup>[[#fn:r459|459]]</sup> ; Sydeman et al., 2015 <sup>[[#fn:r460|460]]</sup> ; Breed et al., 2017 <sup>[[#fn:r461|461]]</sup> ) (see Chapter 3; section 3.2.1.4). In addition, marine mammals, seabirds and sea turtles present habitat requirements associated with bathymetric and mesoscale features that facilitate the aggregation of their prey (Bost et al., 2015 <sup>[[#fn:r462|462]]</sup> ; Kavanaugh et al., 2015 <sup>[[#fn:r463|463]]</sup> ; Hindell et al., 2016 <sup>[[#fn:r464|464]]</sup> ; Hunt et al., 2016 <sup>[[#fn:r465|465]]</sup> ; Santora et al., 2017 <sup>[[#fn:r466|466]]</sup> ). The persistence and location of these features are linked to variations in climate (Crocker et al., 2006 <sup>[[#fn:r467|467]]</sup> ; Baez et al., 2011 <sup>[[#fn:r468|468]]</sup> ; Dugger et al., 2014 <sup>[[#fn:r469|469]]</sup> ; Abrahms et al., 2017 <sup>[[#fn:r470|470]]</sup> ; Youngflesh et al., 2017 <sup>[[#fn:r471|471]]</sup> ) and to foraging success, juvenile recruitment, breeding phenology, growth rates and population stability (Costa et al., 2010 <sup>[[#fn:r472|472]]</sup> ; Ancona and Drummond, 2013 <sup>[[#fn:r473|473]]</sup> ; Ducklow et al., 2013 <sup>[[#fn:r474|474]]</sup> ; Chambers et al., 2014 <sup>[[#fn:r475|475]]</sup> ; Descamps et al., 2015 <sup>[[#fn:r476|476]]</sup> ; Abadi et al., 2017 <sup>[[#fn:r477|477]]</sup> ; Bjorndal et al., 2017 <sup>[[#fn:r478|478]]</sup> ; Fluhr et al., 2017; Youngflesh et al., 2017) ( ''high confidence'' ). Overall, recent evidence further support that impacts of climate change on some marine reptiles, mammals and birds have been observed in recent decades ( ''high confidence'' ) and that the direction of impacts vary between species, population and geographic locations (Trivelpiece et al., 2011; Hazen et al., 2013; Clucas et al., 2014; Constable et al., 2014; George et al., 2015) ( ''high confidence'' ).

Warming has contributed also to observed changes in phenology (timing of repeated seasonal activities) of marine organisms (Gittings et al., 2018 <sup>[[#fn:r505|505]]</sup> ), although observations are biased towards the northeast Atlantic (Poloczanska et al., 2016 <sup>[[#fn:r506|506]]</sup> ; Thackeray et al., 2016). Shifts in the timing of interacting species have occurred in the last decades, eventually leading to uncoupling between prey and predators, with cascading community and ecosystem consequences (Kharouba et al., 2018; Neuheimer et al., 2018 <sup>[[#fn:r507|507]]</sup> ). Timing of spring phenology of marine organisms is shifting to earlier in the year under warming, at an average rate of 4.4 ± 1.1 days per decade (Poloczanska et al., 2013 <sup>[[#fn:r508|508]]</sup> ), although it is variable among taxonomic groups and among ocean regions (Lindley and Kirby, 2010 <sup>[[#fn:r509|509]]</sup> ). This is consistent with the expectations based on the close relationship between temperature and these biological events, supporting evidence from AR5 (Bruge et al., 2016 <sup>[[#fn:r510|510]]</sup> ; Poloczanska et al., 2016 <sup>[[#fn:r511|511]]</sup> ). Thus, the growing amount of literature and new studies since AR5 WGII and SR15 further support   that phenology of marine ectotherms in the epipelagic systems are related to ocean warming ( ''high confidence'' ) and that the timing of biological events has shifted earlier ( ''high confidence'' ).

''Observed impacts of multiple climatic hazards''

WGII AR5 concludes that multiple climatic hazards from ocean acidification, hypoxia and decrease in nutrient and food supplies pose risks to marine ecosystems, and the risk can be elevated when combined with warming (Riebesell and Gattuso, 2014 <sup>[[#fn:r512|512]]</sup> ; Gattuso et al., 2015 <sup>[[#fn:r513|513]]</sup> ). In a recent meta-analysis of 632 published experiments, primary production by temperate non-calcifying plankton increases with elevated temperature and CO 2 , whereas tropical plankton decreases productivity because of acidification (Nagelkerken and Connell, 2015 <sup>[[#fn:r514|514]]</sup> ). Also, temperature increases consumption and metabolic rates of herbivores but not secondary production; the latter decreases with acidification in calcifying and non-calcifying species. These effects together create a mismatch with carnivores whose metabolic and foraging costs increase with temperature (Nagelkerken and Connell, 2015 <sup>[[#fn:r515|515]]</sup> ). Warming may also exacerbate the effects of ocean acidification on the rate of photosynthesis in phytoplankton (Lefevre, 2016 <sup>[[#fn:r516|516]]</sup> ). There is some, but limited, reports of observed impacts on calcified pelagic organisms that are attributed to secular trend in ocean acidification and warming (Harvey et al., 2013 <sup>[[#fn:r517|517]]</sup> ; Kroeker et al., 2013 <sup>[[#fn:r518|518]]</sup> ; Nagelkerken et al., 2015 <sup>[[#fn:r519|519]]</sup> ; Boyd et al., 2016 <sup>[[#fn:r520|520]]</sup> ). For example , Rivero-Calle et al. (2015) reported, using CPR archives, that stocks of coccolithophores (a group of phytoplankton that forms calcium carbonate plateles) have increased by 2% to over 20% in the north Atlantic over the last five decades, and that this increase is linked to synergistic effects of increasing anthropogenic CO 2 and rising temperatures, as supported by their statistical analysis and a number of experimental studies. Most of the available evidence supports that ocean acidification and hypoxia can act additively or synergistically between each other and with temperature across different groups of biota (Figure 5.13). Limitation of nutrient and food availability and predation pressures can further increase the sensitivity of organismal groups to climate change in specific ecosystems (Riebesell et al., 2017 <sup>[[#fn:r494|494]]</sup> ). Climate change also affects organisms indirectly through the impacts on competitiveness between organisms that favour those that are more adaptive to the changing environmental conditions (Alguero-Muniz et al., 2017 <sup>[[#fn:r495|495]]</sup> ) and changes in trophic interactions (Seebacher et al., 2014 <sup>[[#fn:r496|496]]</sup> ). Overall, direct ''in situ'' observations and laboratory experiments show that there are significant responses to the multiple stressors of warming, ocean acidification and low oxygen on phytoplankton, zooplankton and fishes and that these responses can be additive or synergistic ( ''high confidence,'' Figure 5.13).

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