Impacts of Climate Variation and Potential Effects of Climate Change on South American Seabirds Á a Review

Marine Biology Research, 2013 Vol. 9, No. 4, 337Á357, http://dx.doi.org/10.1080/17451000.2012.756982

INVITED REVIEW

Impacts of climate variation and potential effects of climate change on South American seabirds Á a review

PETRA QUILLFELDT* & JUAN F. MASELLO

Justus Liebig University Giessen, Department of Animal Ecology & Systematics, Germany

Abstract The coastal and oceanic waters around the South American coasts provide rich foraging grounds for breeding and wintering seabirds, but there is growing concern that climate change will provide additional pressures to the seabirds around South America. As in many other coastal ecosystems, seabirds around South America are already faced with threats to their breeding habitats such as human disturbance and introduced predators, and threats at sea such as persistent pollutants and pesticides and direct mortality risks due to fisheries and oil spills. The sensitivity of South American marine ecosystems to ocean climate anomalies is well known from the dramatic population collapses caused by El Nin˜o Southern Oscillation (ENSO) events. However, longer-term climate change effects have been explored less often and few long-term data sets exist for South American seabirds. Seven Large Marine Ecosystems (LME) border South America. While all LMEs experienced warming during the last 50 years, their climate dynamics have differed in recent decades. Climate models suggest that potential climate change effects may be important, especially due to changes in ENSO intensity and frequency and associated changes in the ocean climate of Atlantic and Pacific marine ecosystems. In this review, we found that the best studied seabird communities are those of the Patagonian Shelf and the Humboldt Current, but overall, our knowledge on climate effects on South American seabirds is scarce.

Key words: Aves, climate change, ENSO, South America, coastal ocean ecosystems

Introduction incidence of disease (Hoegh-Guldberg & Bruno 2010). Several recent reviews suggested that global Anthropogenic climate change affects the physical warming has a profound bottom-up impact upon environment of seabirds through increasing air and ocean temperatures (Levitus et al. 2000, 2005) marine top-predators (e.g. Gre´millet & Boulinier and associated changes in patterns of precipitation 2009; Chambers et al. 2011). Climate change also and changes in frequency and severity of extreme increasingly affects seabirds. It has been estimated events (e.g. Timmermann et al. 1999; Holmgren that adverse weather and climatic events at breeding sites and the potential impact of sea level rise Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 et al. 2001; Cobb et al. 2003). Rising atmospheric greenhouse gas concentrations have increased glo- negatively influence the conservation status of 40% bal average temperatures by about 0.28C per decade of the 97 globally threatened seabird species, making over the past 40 years (Hansen et al. 2010), and it the third most common threat after invasive alien much of this added energy is absorbed by the world’s species and bycatch (Croxall et al. 2012, fig. 7). oceans. As a result, the average temperature of the Long-term observations of seabirds show that upper layers of the ocean has increased by 0.68C increases in sea surface temperature (SST) typically over the past 100 years (IPCC 2007). Measurable cause low availability of seabird prey, and conse- impacts of this ocean climate change so far include quently deferred reproduction, lowered growth rates decreased ocean productivity, altered food web and high mortality of chicks in different oceans such dynamics, reduced abundance of habitat-forming as the Antarctic (Jenouvrier et al. 2005b; Le Bohec species, shifting species distributions, and a greater et al. 2008), the Indian Ocean (Monticelli et al. 2007),

*Correspondence: Petra Quillfeldt, Justus Liebig University Giessen, Department of Animal Ecology & Systematics, Heinrich-Buff-Ring 38, D-35392 Giessen, Germany. E-mail: [email protected] Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory, University of Copenhagen, Denmark

(Accepted 22 November 2012; Published online 18 February 2013) # 2013 Taylor & Francis 338 P. Quillfeldt and J. F. Masello

the North Atlantic (Durant et al. 2004; Riou et al. seabirds (e.g. California Current: Ainley & Hyrenbach 2011) and the Southern Ocean (Weimerskirch et al. 2010). 2003). Thus, global ocean warming places an added Responses of seabirds to either climate change or, burden on many seabird species (e.g. Ainley et al. more specifically, warm SST, include increased 2010), although some seabirds have also been shown mortality levels (e.g. southern fulmar Fulmarus to benefit from climatic change (e.g. Hamer 2010; glacialoides (Smith, 1840), in 1964Á2002: Jenouvrier Rivalan et al. 2010; Weimerskirch et al. 2012). et al. 2003; emperor penguin in 1962Á2001: Most seabirds feed at a relatively narrow range of Jenouvrier et al. 2005a; King penguin Aptenodytes trophic levels, mainly taking larger zooplankton or patagonicus Miller, 1778, in 1997Á2005: Le Bohec small pelagic fish or squid. Most seabird prey is thus et al. 2008; Northern Atlantic seabirds in 1989Á2003: strongly influenced by climate-driven changes in Sandvik et al. 2005; Gala´pagos penguins Spheniscus phytoplankton productivity (e.g. Behrenfeld et al. mendiculus Sundevall, 1871, in 1971Á2004: Vargas 2006), which cause changes in the abundance and et al. 2006), changes in migration patterns (sooty fecundity of small grazing zooplankton such as shearwater Puffinus griseus (Gmelin, 1789), in 1987Á copepods and euphausiids and in consequence, 1994: Veit et al. 1996) and changes in the distribu- carnivorous zooplankton and pelagic fish or squid. tion of species (e.g. non-breeding species in the The dynamics of small pelagic fish has been studied California upwelling system: Ainley et al. 2005; intensively in upwelling ecosystems, such as the South Africa: Crawford et al. 2008b), changes in Humboldt and Benguela currents, where collapses the phenology of breeding (e.g. kittiwakes Rissa of small pelagic fish populations are often accom- tridactyla (Linnaeus, 1758), in 1955Á1987: Aebischer panied by sharp declines in marine bird populations et al. 1990; and in 1970Á2008: Moe et al. 2009; (Crawford & Jahncke 1999; Crawford et al. 2008a). blue-footed booby Sula nebouxii Milne-Edwards, Most seabirds have life-history characteristics that 1882, in 1989Á2006: Ancona et al. 2011; Antarctic buffer their populations against interannual fluctua- seabirds in 1950Á2004: Barbraud & Weimerskirch tions in their food sources, such as high survivorship 2006; little auks Alle alle (Linnaeus, 1758), in 1963Á and longevity. However, longevity comes at the cost 2008: Moe et al. 2009), reduced breeding parti- of low fecundity, such that population recovery is cipation (e.g. blue-footed booby in 1989Á2006: usually low. Furthermore, seabirds are restricted Ancona et al. 2011; red-footed booby Sula sula to specific breeding sites such as predator-free is- (Linnaeus, 1766), in 1983Á2002: Cubaynes et al. lands, from where they act as central-place foragers. 2011), reduced breeding success (e.g. kittiwakes in Depending on their mode of locomotion (gliding 1955Á1987: Aebischer et al. 1990; tufted puffins or flapping flight, or underwater pursuit diving), Fratercula cirrhata (Pallas, 1769), in 1975Á2002: foraging is more or less energetically costly and the Gjerdrum et al. 2003) and reduced offspring quality foraging range more or less restricted. Thus, seabird (e.g. tufted puffins in 1975Á2002: Gjerdrum et al. guilds would be expected to differ in their ability to 2003). respond to a shift in prey distribution. Few studies From the list above, it becomes clear that long- have tested this hypothesis (e.g. Jaksik & Farin˜a term data sets have been crucial for understanding 2010). these changes; and that these long-term data sets are Climate change effects can also be significant for mainly concentrated around Antarctica, North Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 high-latitude seabirds. Antarctic penguin species America and Northern Europe (e.g. Sandvik & adapted to sea-ice habitat are among those where Erikstad 2008 for a meta analysis in the North large effects are expected. For example, a simulation Atlantic; Sydeman et al. 2012 for a global analysis), of a 28C warmer climate predicts that 50% of while only one of these data sets originates from emperor penguin (Aptenodytes forsteri Gray, 1844) South America (Vargas et al. 2006). However, South colonies (40% of breeding population) and 75% of America also harbours important breeding sites for Ade´lie penguin (Pygoscelis adeliae (Hombron & seabirds (e.g. Yorio et al. 1999; Simeone et al. 2003) Jacquinot, 1841)) colonies (70% of breeding popu- and oceanic and/or coastal areas offer wintering sites lation) will disappear (Ainley et al. 2010). for Antarctic and Sub-Antarctic seabirds (reviewed Changes in climatic conditions can therefore cause by Costa et al. 2011) as well as Northern Hemi- dramatic changes in food availability, followed by sphere seabirds (e.g. Spear & Ainley 2008). In the changes in population size, distribution or reproduc- subsequent sections, we summarize the state of tive ecology of seabirds (e.g. Kitaysky & Golubova knowledge on seabird responses to climatic varia- 2000; Jaksic 2004). There are signs that ocean bility in South American waters, using the units of warming and acidification decreases the carrying the Large Marine Ecosystems (LMEs) to structure capacity of many marine ecosystems and this is the review. We give a detailed account on three reflected in the decreasing population sizes of LMEs (Humboldt Current, Patagonian Shelf and Impacts of climate variation on South American seabirds 339

South Brazil Shelf), from where some studies of LMEs embracing the cold Falkland/Malvinas and seabird responses to climate have been reported. the warmer Brazil currents. In an analysis of LMEs, there was a widespread, global pattern of warming in the period 1957Á2006 South American Large Marine Ecosystems and (Sherman & Hempel 2009). This also affected all climate seven South American LMEs, although to varying Large Marine Ecosystems are ocean areas of ap- degrees. proximately 200,000 km2 or greater, adjacent to the There is growing awareness that environmental continents in coastal waters where primary produc- variability plays a crucial role in marine ecosystems. tivity is generally higher than in open ocean areas Global climatic phenomena cause environmental (e.g. Sherman 1991). The extent of the LME is variability in South American waters. In particular, defined by four linked ecological criteria: bathy- the El Nin˜o Southern Oscillation (ENSO) and the metry, hydrography, productivity and trophic rela- Antarctic Oscillation (AAO) are climatic cycles that tionships. A total of 64 distinct LMEs have been greatly affect vast regions of South America and the delineated around the world’s ocean coasts, 7 of surrounding oceanic waters (e.g. Ropelewski & them around South America (Figure 1). South Halpert 1987, 1989; Silvestri & Vera 2003). Re- America is bordered by the Pacific Ocean with the search in the last two decades has shown that ENSO southernmost portion of the Pacific Central-Amer- has major implications for the functioning of eco- ican coastal LME and the cold Humboldt Current systems and pulses of primary productivity that can LME in the west. Several northwestern South cascade upward through the food web invoking American countries border the Caribbean Sea, and unforeseen feedbacks (e.g. terrestrial ecosystems: the Atlantic Ocean coasts are separated into four Jaksic et al. 1997; Holmgren et al. 2001, 2006). Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013

Figure 1. Large Marine Ecosystems bordering South America, as deﬁned by Sherman & Hempel (2009) (see also http://www.lme.noaa. gov/). 340 P. Quillfeldt and J. F. Masello

ENSO is the strongest climate signal of global lation Index (SOI) summarizes the state of the impact that affects marine ecosystems, by changing ENSO on a global scale, and appears to be strongly patterns of upwelling with a frequency of 3Á7 years related to the breeding success and survival of (e.g. Timmermann et al. 1999; Dijkstra 2006; Ashok seabirds ranging widely, such as albatrosses and & Yamagata 2009; Yeh et al. 2009). El Ninõ years many petrels (e.g. Nevoux et al. 2007; Rolland are defined by warmer than normal SSTs in the et al. 2010). eastern tropical Pacific, depressing primary produc- Chambers et al. (2011) pointed out further tivity and consequently the trophic web depending potential impacts of climate change, including effects on primary production. Although El Ninõ is the of rises in sea level and storms, ocean acidification, classic example of the impact of climate variability changing wind patterns, increased land temperature on ocean ecosystems (Barber & Chavez 1983), and extreme precipitation events. longer and more gradual changes in marine environ- Rises in sea level may cause flooding of seabird ments are also important and can cause profound colonies on low-lying islands and atolls, or increased changes on marine living resources (e.g. Alheit & competition for nesting space as island size is Niquen 2004) leading to the so-called ‘regime-shifts’ reduced. Urban developments of islands and coastal once they reach a tipping point. areas will constrain the ability of seabirds to find While we will discuss impacts of ENSO cycles alternative nesting locations, or lead to seabirds mainly within the Humboldt Current LME, it is breeding on artificial structures (e.g. Erwin 1980; important to notice that changes in SST related to Coulson & Coulson 2008). However, some birds the ENSO cycle occur also in places far from the may also benefit from climate-driven habitat mod- source of the phenomenon, i.e. outside of the Pacific ifications. Some indirect evidence comes from coast- (e.g. Ropelewski & Halpert 1987; Holmgren et al. al waterbirds: several species of herons breeding in 2001, 2006), and that several climate models predict mangrove habitats recently expanded southwards in an increased frequency or change in the pattern of Brazil (Gianuca 2007; Gianuca et al. 2008). ENSO cycles with climate change (e.g. Timmermann Altered wind patterns can have effects on food et al. 1999; Yeh et al. 2009). availability, especially for far-ranging, surface-feed- The ENSO cycle is present in all relevant paleo- ing seabirds (e.g. wandering albatross Diomedea climate records. It was systematically weaker during exulans Linnaeus, 1758: Weimerskirch et al. 2012). the early and middle Holocene, and data from corals Storms, increased land temperature and extreme show substantial decadal and longer variations in the precipitation events may lead to increased breeding strength of the ENSO cycle within the past 1000 failures if they affect the breeding sites. Taken years (Cane 2005). Models used for future climate together, these parameters could profoundly alter projections provide an indeterminate picture of biodiversity and ecosystem functioning in many ENSO’s future. Some predict more ENSO activity regions of the world, as populations may not be (e.g. Timmermann et al. 1999), but some also less able to respond as fast as the changing conditions (reviewed in Cane 2005). A puzzling shift in the might require. ENSO cycle behaviour was observed over recent Seabirds face a number of imminent threats, years (Yeh et al. 2009), with a distinction among which may seem more urgent than gradual climate ‘classic’ Eastern Pacific (EP) El Ninõ and the new change and its associated climatic phenomena. In Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 phenomenon the Central Pacific (CP) El Ninõ, particular, fisheries over-exploitation, pollution where the maximum SST anomaly persists in the (especially oil), introduced species, habitat destruc- central Pacific from the boreal summer through to tion and human disturbance through coastal devel- the winter. The occurrence ratio of the CP-El Ninõ opment, guano harvesting and tourism are especially to the EP-El Ninõ is expected to increase in response relevant (e.g. Yorio et al. 1999; Petry & Fonseca to global warming (Yeh et al. 2009), and the 2002; Tourinho et al. 2010). Offshore fishing importance of this change for seabirds remains to operations may provide food in the form of discards be explored. (Bugoni et al. 2010), but also lead to incidental Impacts of ENSO on reproduction of seabird mortality of penguins, albatrosses, petrels, shear- populations have been detected in places far from waters and cormorants (e.g. Favero et al. 2003; the equatorial Pacific, where they often occur after a Phillips et al. 2006; Gonza´lez-Zevallos & Yorio 2006; lag of few months or years (e.g., Ainley et al. 1995; Bugoni et al. 2008a; Jimeńez et al. 2009; Cardoso Guinet et al. 1998; Chambers 2004; Quillfeldt et al. et al. 2011) and to increased intake of heavy metals 2007), depending on the distance of the site from the (Carvalho et al. 2013). While some of these threats equatorial Pacific and on the time required for are locally restricted or could be remedied through bottom-up processes to cascade to upper trophic political decisions, climatic phenomena have the levels (Monticelli et al. 2007). The Southern Oscil- potential to influence the whole region profoundly Impacts of climate variation on South American seabirds 341

and add to the cumulative pressure affecting many 1837)) and Peruvian pelican (Pelecanus thagus seabird species. Molina, 1782) (e.g. Croxall et al. 1984). In addition, over 90 species of seabirds were recorded offshore (Spear & Ainley 2008), composed of 18 endemics, Humboldt Current LME 10 residents (species breeding in the study area The Humboldt Current along the Pacific coasts of and elsewhere), 41 Southern Hemisphere migrants Chile and Peru is the world’s largest coastal upwel- (most numerous: black-browed albatross T. mela- ling system. Intense wind-induced upwelling cells nophris (Temminck, 1828), white-chinned petrel along the coast result in unusually cool surface Procellaria aequinoctialis Linnaeus, 1758, Juan waters, relative to latitude. For example, the SST Fernandez petrel Pterodroma externa (Salvin, 1875), at 58S off Peru is as cool as 168C when most other thin-billed prion Pachyptila belcheri (Mathews, tropical locations are in excess of 258C (Chavez et al. 1912), blue-footed booby Sula nebouxii, 18 North- 2008). In addition, the surface oxygenated waters in ern Hemisphere migrants (most numerous: red the Humboldt Current overlie an intense and phalarope Phalaropus fulicarius (Linnaeus, 1758), extremely shallow Oxygen Minimum Zone that Franklin’s gull Larus pipixcan (Wagler, 1831) and 6 forms a barrier and concentrates living resources migrants that breed in both hemispheres. The most near the surface, thus making them available for common species was the sooty shearwater (Spear & seabirds. Ainley 2008). Characteristic resident seabirds (Figure 2) include The southern part of the Humboldt Current LME Humboldt penguins (Spheniscus humboldti Meyen, differs in several aspects from the more northern 1834), Peruvian diving petrels (Pelecanoides garnotii coasts with their relatively linear, arid coastline and (Lesson, 1828)) and the so-called guano birds: few rocky islands. The southern Chilean waters are Peruvian booby (Sula variegata (Tschudi, 1845)), characterized by many islands, fjords and channels, guanay cormorant (Phalacrocorax bougainvilii (Lesson, but which remain poorly studied and inaccessible, Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013

Figure 2. Humboldt Current LME seabirds: Humboldt penguins (upper left), Peruvian boobies (upper right), Chilean pelicans (lower left) and red-legged cormorants (lower right). Choros and Chungungo Islands, Northern Chile. Photographer: Petra Quillfeldt. 342 P. Quillfeldt and J. F. Masello

with a coldÁhumid climate and partly dense vegeta- 1991) as well as Humboldt penguins (Culik 2001). tion (e.g. Croxall et al. 1984). The seabirds are Adult seabirds often did not attempt to breed (e.g. clearly more Sub-Antarctic, with similar species to Jahncke & Goya 1998; Zavalaga et al. 2008), and if seabirds in the Patagonian shelf LME. For the so, chicks were fed less than usual (e.g. Ainley et al. purposes of this review, we also count the Gala´pagos 1988). In Gala´pagos penguins, breeding attempts Islands as part of the Humboldt LME, as its climate failed during most El Ninõ events, and the strongest variability is similar to that of the coast, being part of events in 1982Á1983 and 1997Á1998 caused mor- the extended Humboldt Current upwelling system. tality of adults from starvation and a population The average primary productivity in the Hum- decline by an estimated 77% and 65%, respectively boldt Current LME is moderate, however, the (Rosenberg & Harcourt 1987; Vargas et al. 2006), northern Humboldt Current system off Peru pro- followed by slow recovery (Boersma 1998). Today, duces more fish per unit area than any other region Gala´pagos penguin numbers are only about 25% in the world oceans (Chavez et al. 2008), represent- of what they were in the 1970s (Boersma 2008). ing less than 0.1% of the world ocean surface but In central Chile, the number of breeding pairs presently producing about 10% of the world fish of Neotropic cormorants (Phalacrocorax brasilianus catch. The fishery, as well as the seabirds, depend on (Gmelin, 1789)) declined by 71% during El Ninõ, a crucial intermediate trophic level of small, plank- laying started 15 days later, was less synchronized ton-feeding pelagic fish dominated by a few school- and ended 35 days later (Kalmbach et al. 2001). Not ing species, especially Peruvian anchoveta (Engraulis only did the pelagic fish migrate to deeper, inacces- ringens Jenyns, 1842) and Pacific sardines (Sardinops sible waters, reducing the food availability, but an sagax (Jenyns, 1842)). Their massive populations increase in rainfall (e.g. Kane 1999; Andreoli & may vary radically in size, depending on the available Kayano 2005) and rising sea levels also contributed primary productivity. About 94% of the variation in to seabird breeding failures (e.g. Valle et al. 1987). In guanay cormorant and Peruvian booby numbers central Chile, 55Á85% fewer breeding pairs of from 1925 to 2000 were explained by two factors Humboldt penguins were present at the breeding governing primary production in the Humboldt colonies during the 1997/98 El Ninõ episode, the upwelling system, namely wind stress and SST, onset of nesting was delayed, and abnormally heavy and the competitive effect of the fishery that limits rainfall flooded nests (Simeone et al. 2002). While prey availability (Jahncke et al. 2004). The Hum- the number of breeding pairs was significantly related boldt Current is affected by strong seasonal, inter- to sea surface temperature anomalies (SSTA), breed- annual and longer-term variability. In particular, the ing success was not. Humboldt Current is well known for the periodic There is some evidence that the ecology and life occurrence of ENSO. During the warmest phase, El history of seabirds influences the degree to which El Ninõ conditions, the upwelling can be interrupted Ninõ events affected different species. Seabirds with and primary productivity depressed. Occurrences of a narrow dietary range (e.g. those eating fish and fish ENSO are associated with large-scale changes in larvae) were the most severely affected by El Ninõ seabird geographic distribution, survival, and repro- 1982Á1983 (Jaksik & Farinã 2010). This relation- ductive success in the Humboldt Current (reviewed ship is also found within species, for example SSTAs by Jaksik & Farinã 2010). Strong declines of seabird were negatively correlated with diet diversity in Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 populations along Peruvian and Chilean coasts and Peruvian diving petrels, suggesting that warm con- in the Gala´pagos Islands have been associated with ditions decrease prey options (Garc´ıa-Godos & Goya El Ninõ events (e.g. Anderson 1989; Boersma 1978; 2006). Further, seabird populations can recover Kalmbach et al. 2001). This link between oceano- rapidly after El Ninõ if they have large clutch sizes, graphic events and seabird breeding failures and die- fast body growth rates and early reproductive ages. offs has been observed for a long time (Murphy In the Humboldt Current system, the seabird 1926), and has more recently been studied intensely, assemblages are dominated by species with these when one of the most severe El Ninõ events occurred life history characteristics (Luna-Jorquera et al. during 1982Á1983, as well as during the El Ninõ 2003). Thus, response to El Ninõ could be an event of 1997Á1998. Responses included movement important selective factor for breeding biology and away from Peruvian waters during El Ninõ events life-history patterns of seabirds. (e.g. Mackiernan et al. 2001) and large numbers of El Ninõ events have always had a negative dead and dying birds at several places throughout influence on guano bird populations, but severe the eastern Pacific (Ainley et al. 1988, Duffy 1990). crashes have only been apparent since fishing ENSO-related southward migration of top-predators activities intensified (Croxall et al. 1984). In addi- relying on the Humboldt Current ecosystem has tion, it has been observed that anchovy can recover been observed in guano birds (Arntz & Fahrbach even from strong ENSO events within 1Á2 years and, Impacts of climate variation on South American seabirds 343

therefore, periods of warm and cold temperature In summary, Humboldt Current seabird work has anomalies on the decadal scale seem to play a more mainly concentrated on the impact of extreme El important role for long-term anchovy dynamics than Ninõ events, while systematic long-term data sets on ENSO events (Alheit & Niquen 2004). Further- seabird demographics in the Humboldt Current are more, a recent model simulates a cooling trend of the lacking. It has been pointed out that by concentrat- SST off Peru, with an increase in the occurrence of ing efforts only on El Ninõ years (e.g. 12 years the CP El Ninõ events but a reduction of EP El Ninõ during the last century: Jaksik & Farinã 2010), we and, thus, mesoscale El Ninõ activity in the northern are missing the information of the ‘normal’ years, Humboldt Current region (Dewitte et al. 2012). If which is essential for understanding not only the these model predictions are correct, seabirds in this responses of birds during the ENSO cycle, but also region may have a favourable time ahead. the influence of the warm and cold temperature In the 1950sÁ1970s, seabird numbers collapsed anomalies on the decadal scale. after a large-scale commercial fishery reduced anchoveta stocks in the northern Humboldt Current. However, at the same time, waters became warmer, Patagonian Shelf LME most likely causing a regime shift (e.g. Cahuin et al. The waters of the Patagonian Shelf, one of the 2009). Thus, it has been proposed that the long- widest shelves in the world, support a highly pro- term dynamics of the Humboldt Current ecosystem ductive marine ecosystem ( 300 gC/m2-yr based are controlled by shifts between alternating anchovy on SeaWiFS global primary production estimates, and sardine regimes (Alheit & Niquen 2004). Such e.g. Carranza et al. 2008; Sherman & Hempel regimes are caused by lasting periods of warm or 2009). The Patagonian Shelf extends from Tierra cold temperature anomalies and restructure the del Fuego in the south to the Rio de la Plata River entire ecosystem from phytoplankton to the top in the north, encompassing the Atlantic coast of predators. Phases with colder water temperatures Argentina, and large islands in the south (Staten parallel anchovy regimes (termed ‘La Vieja’, e.g. Island, Falkland/Malvinas Islands; e.g. Glorioso 1950Á1970; 1985 to the present). During a warmer 2002; Piola 2008). In the southern part of the period from 1970 to 1985 (termed ‘El Viejo’), Patagonian Shelf, high primary production is sup- sardines became dominant as anchovy populations ported by upwelling of cold Antarctic waters. The were restricted to smaller coastal upwelling cells for cold, northward Falkland/Malvinas Current extends feeding and spawning, increasing egg and larval along the Patagonian Shelf break and provides an cannibalism and predation, and anchovy catchability ecological border to the east. The northern part of (Alheit & Niquen 2004; Chavez et al. 2008). The the Patagonian Shelf is dominated by the subtropi- example shows how small pelagic fish such as sardine cal, southward Brazil Current, which is higher in and anchovy respond dramatically and quickly to temperature and salinity and supports lower pro- changes in ocean climate, causing dramatic changes ductivity (e.g. Stramma 1989; Piola 2008). Where in abundance over a few decades. A number of the two currents meet, they form an extensive and seabird species (e.g. Salvin’s Thalassarche salvini highly productive confluence zone (e.g. Gordon (Rothschild, 1893), and black-browed albatrosses, 1989; Peterson & Stramma 1991; Seeliger et al. southern fulmars, white-chinned and pintado 1991), which is also influenced by the outflow of Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 (Cape) petrels Daption capense (Linnaeus, 1758), the Rio de la Plata River, the second largest drainage Wilson’s storm-petrels Oceanites oceanicus (Kuhl, in South America. In addition to these boundary 1820) and thin-billed prions) moves into the LME currents, the extent of the Patagonian Shelf allows mostly from the Antarctic and Sub-Antarctic, ap- for the development of a great diversity of mesoscale pearing during winter and then remaining in colder, fronts (Acha et al. 2004), including a number of less saline waters (Spear & Ainley 2008). On a year-round and seasonal tidal fronts, such as the smaller spatial scale, a major upwelling area with low Bah´ıa Grande Front and the Valde´s Front. These SST in the southern part of the Coquimbo area in fronts play a paramount role in ecological processes, northern Chile attracted Juan Fernandez petrels, allowing for high biological production, offering Antarctic prions Pachyptila desolata (Gmelin, 1789), feeding and/or reproductive habitats for fishes, and white-chinned petrels (Weichler et al. 2004). squids, and birds (Acha et al. 2004; Orgeira 2001). Likewise, cold-water areas in the Gala´pagos Archi- Argentine anchovy (Engraulis anchoita Hubbs & pelago attracted a number of seabirds, such as storm Marini in Marini, 1935) is the main pelagic species petrels and boobies (Hayes & Baker 1989). Given in the northern Patagonian shelf LME and the these preferences for cold-water areas, interannual preferred food of many seabirds from southern variability in ocean climate would affect the offshore Brazil to Patagonia (e.g. Skewgar et al. 2003). The distribution and abundance of seabirds in the LME. Patagonian stock spawns during late spring and 344 P. Quillfeldt and J. F. Masello

summer in association with tidal frontal systems. (e.g. Padovani et al. 2012) and thus, along with the The annual anchovy larval density off Patagonia Chilean sprat (Sprattus fuegensis (Jenyns, 1842)), it is depends on the formation of these systems, and another key species in the trophic dynamics of varies interannually by an order of magnitude Austral Patagonia (Sabatini & A´ lvarez-Colombo (Pa´jaro et al. 2009). Further south, squid share the 2001). ecological niche of epipelagic fish on the Falkland Due to the complex oceanography, the biological Shelf and Slope (Laptikhovsky et al. 2010). The diversity of the Patagonian shelf LME is high, with hyperiid amphipod Themisto gaudichaudii Gue´rin- cold- and warm-water adapted species. Character- Me´neville, 1825 is a crucial food item for many of istic breeding seabirds (Figure 3) thus include the fish and squid species distributed in the region (Sub-)Antarctic species such as black-browed Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013

Figure 3. Patagonian Shelf LME seabirds. Upper row left to right: imperial shag, gentoo penguin, dolphin gull, southern rockhopper penguin. Second row: breeding sites on cliffs (left, New Island) and beaches (right, Pen´ınsula Valde´z). Third row: mixed breeding colonies (here, southern rockhopper penguins, black-browed albatrosses and imperial shags). Lower row left to right: Falkland skua, Magellanic penguin, black-browed albatross, thin-billed prion. Falkland Islands/Islas Malvinas and Pen´ınsula Valde´z. Photographer: Petra Quillfeldt. Impacts of climate variation on South American seabirds 345

albatross, imperial shags (Phalacrocorax atriceps of the circumpolar vortex, may also have an influ- King, 1828), Wilson’s storm-petrels, southern rock- ence (Silvestri & Vera 2003). hopper penguins (Eudyptes chrysocome (Forster, SSTAs have been shown to influence seabirds in 1781)) and gentoo penguins (Pygoscelis papua (For- the Sub-Antarctic Falkland/Malvinas Islands. SST ster, 1781)), temperate species such as Magellanic anomalies were negatively correlated with provision- penguins (Spheniscus magellanicus (Forster, 1781)), ing rates and chick growth in thin-billed prions dolphin gulls (Larus scoresbii Traill, 1823) and rock (Quillfeldt et al. 2007, 2010b) and showed a quad- shags Phalacrocorax magellanicus (Gmelin, 1789)) ratic relationship with southern rockhopper pen- (e.g. Croxall et al. 1984; Yorio 2000). Penguin guin survival rates (Dehnhard et al. in press). populations are especially important, an order of Winters that are colder than the current average magnitude larger than the rest on the coasts of provide optimal oceanographic conditions, where Argentina (Yorio et al. 1999), but many popula- southern rockhopper penguins were able to find tions have declined in the last decades both in enough food to survive and prepare for the following Argentina (Boersma 2008) and in the Falkland/ breeding season (Raya-Rey et al. 2007). A study of Malvinas Islands (Pu¨tz et al. 2003). At the same the influence of SST on gentoo penguin numbers time, some actually show an increase and the breed- indicated a non-linear response and differences ing range is expanding to the north, suggesting that among areas (Baylis et al. 2012). This might reflect these regional differences potentially depend on the differences in trophic level and foraging ecology, oceanographicÁclimatic factors. but also in the timescale of measurements taken. Petrels also breed in large numbers, especially in Gentoo penguins mainly feed on fish and squid that the Falkland/Malvinas Islands. Of five regularly occur close to their breeding sites (e.g. Masello et al. observed albatross species, only the black-browed 2010), and the abundance of their prey is influenced albatross breeds in the area and is resident year- by environmental variability (Waluda et al. 1999, round. The Patagonian shelf LME further offers 2004), which may vary locally across the archipelago. important foraging areas for seabirds breeding at In contrast, thin-billed prions and rockhopper pen- adjacent island groups such as South Georgia in the guins feed on zooplankton and range widely over the Atlantic and Diego Ramirez in Chile (e.g. wandering Patagonian Shelf and, in the case of the prions, into albatross, grey-headed albatross Thalassarche the Drake Passage to the south. Thus, they are able chrysostoma (Forster, 1785), light-mantled albatross to buffer the adverse effects of poor food availability Phoebetria palpebrata (Forster, 1785) and white- with lower provisioning and growth rates. Moreover, chinned petrels: Croxall & Wood 2002). Birds from due to flexible growth rates the chick survival to more distant island groups, e.g. Tristan da Cunha fledging is not necessarily affected by poor condi- and Gough, also feed in Patagonian shelf waters tions (Quillfeldt et al. 2007), and thus any effect on during both breeding and non-breeding seasons numbers of breeding birds would depend mainly on (Croxall & Wood 2002). Further wintering seabirds the survival rate of fledglings and might not be include southern fulmars and Cape petrels from apparent for several years. Antarctic and Sub-Antarctic breeding sites and Some evidence suggests that seabirds of the northern royal albatross (Diomedea sanfordi Murphy, central and northern Patagonian Shelf are also 1917) from New Zealand, while other species such influenced by climate change. The largest Magella- Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 as Wilson’s storm petrels and great shearwater nic penguin colony is located in temperate waters, at (Puffinus gravis (O’Reilly, 1818)) use it as a staging Punta Tombo, Argentina. The breeding population ground on migration. Even birds of the Northern here declined in the last decades (Boersma 2008). In Hemisphere winter here, such as Arctic terns (Sterna the 1980s and 1990s, petroleum pollution was a paradisaea Pontoppidan, 1763), Manx shearwaters major source of Patagonian penguin mortality, but (Puffinus puffinus (Bru¨nnich, 1764)), Cory’s shear- even though this is now less important, the decline waters (Calonectris borealis (Cory, 1881)) and several continues. Climate-driven factors may now become Arctic skuas/jaegers (Favero & Silva-Rodr´ıguez 2005). more important. On one hand, high mortality here The southern Patagonian Shelf waters are domi- was observed in years with severe rains, as many nated by strong westerly winds. Wind-driven cold- chicks die during flooding of nesting burrows water current systems such as the Falkland/Malvinas (Boersma 2008). The area experiences increased Current are strongly affected by climate forcing. For rain during El Nin˜o years (e.g. Ropelewski & example, ENSO-mediated SSTAs generated in the Halpert 1987; Holmgren et al. 2001; Andreoli & Pacific propagate to the Southwest Atlantic with a Kayano 2005). On the other hand, longer foraging lag of 2Á3 years via the Antarctic Circumpolar trips during incubation more than a decade ago Current (Waluda et al. 1999); furthermore, the indicate reductions in prey abundance closer to the Antarctic Oscillation, i.e. fluctuations in the strength colony (Boersma 2008). This may be due to shifts in 346 P. Quillfeldt and J. F. Masello

prey location or a general reduction in productivity historically (45% in 1913Á1915) and have only in response to climate change, but also due to recently become dominant (92% in 2003Á2005), commercial fishing. These causal relationships still apparently in response to warming sea temperatures need to be better understood. and less favourable conditions over the Patagonian As in Argentina, severe weather can also impact Shelf (Quillfeldt et al. 2010a). seabird colonies in the Falkland/Malvinas Islands. Thus, the most relevant datasets on seabird Storms with severe rain caused breeding failures responses to climate in the Patagonian Shelf LME affecting southern rockhopper penguins, imperial come from thin-billed prions and gentoo penguins of shags and black-browed albatross at New Island in the Falkland/Malvinas Islands and from Magellanic January 2008 (Demongin et al. 2010), and black- penguins in Argentina. Although the Patagonian browed albatross and southern rockhopper penguins Shelf experienced only a slight gradual warming at Steeple Jason and Beaucheˆne islands in December during the last 50 years (Table I), the seabird data 2010 (Crofts et al. 2011). For example, the breeding collectively suggest significant changes in the food success of black-browed albatrosses at Steeple Jason base for top-predators of the Patagonian Shelf LME. fluctuated between 40.5% in 2005 and 62% in 2009 These have so far mainly been interpreted as a and decreased to 20% in 2010 due to the impacts of consequence of top-down effects due to commercial the storm, while southern rockhopper penguins at fisheries (e.g. Foro para la Conservacio´n del Mar Steeple Jason failed completely (Crofts et al. 2011). Patago´nico y A´ reas de Influencia 2008). With a predicted increase in storm events and However, several papers suggested changes of the precipitation due to climate change (e.g. Wentz low atmospheric circulation in the Southwest Atlan- et al. 2007; D’Onofrio et al. 2008), an increase in tic during recent decades, such as a poleward shift of frequency of these impacts and the cumulative 38 in the maximum wind zone associated with the effects of other threats is possible. circumpolar westerlies during the period 1976Á1991 Historical changes in at-sea distribution provide (Gibson 1992) and an increase in wave height another line of evidence for climate change effects (Dragani et al. 2010). Strengthening of the circum- acting in this area. In winter, most thin-billed prions polar westerlies and their poleward movement dur- breeding at the Falkland/Malvinas Islands move ing the past 50 years has been shown to favour towards more polar waters (Quillfeldt et al. 2008). wandering albatrosses in the Sub-Antarctic Indian Carbon stable isotope ratios in recent and historical Ocean (Weimerskirch et al. 2012), while their impact feather samples indicated that poleward winter on seabirds in the southwest Atlantic merits atten- movements of thin-billed prions were less common tion. Also, an increase in primary productivity has

Table I. Overview of the oceanographic characteristics of the LMEs (as in Abstract) treated in detail in this review.

Surface Sea surface area temperature trend Geographic (million Protection (warming since LME position Key oceanographic characteristics km2) (%) Productivity 1957; 1982)1

Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 Humboldt West coast of World’s largest coastal upwelling 2.5 0.1 Moderate Variable: Current Chile (558S) to system, intense wind-induced (150Á300 0.418C, 0.108C LME Peru (58S) upwelling cells result in productive gC/m2-yr) cold water masses Patagonian Coast of wide, shallow shelf, with mesoscale 1.2 0.18 Moderate Very gradual Shelf LME Argentina to tidal mixing fronts (e.g. Valde´zf., (150Á300 warming: Uruguay (348S) Bah´ıa Grande f.) and boundary gC/m2-yr) 0.158C, 0.088C currents (Brazil C., Malvinas/Falkland C.), influence of Sub-Antarctic and estuarine waters South Brazil From central Wide (up to 220 km) Shelf, 3 parts: 0.6 1.7 Moderate Moderate warming: Shelf LME Brazil (228S) to a. Southern Shelf influenced by (150Á300 1.128C, 0.538C Uruguay (348S) estuarine outflows, most productive gC/m2-yr) in summer b. South Brazil Bight (seasonal upwellings and cold intrusions) c. Eastern slope (mesoscale eddies, fronts best defined April to September)

1 Linear SST trend since 1957 and 1982 (Sherman & Hempel 2009). Impacts of climate variation on South American seabirds 347

been suggested for the Patagonian Shelf (Gregg et al. marine turtles, cetaceans and seabirds (Neves et al. 2005), which may be attributed, at least in part, to 2006). The seasonally high productivity results in a high nutrient input from glacial flour (as Patagonian considerable biomass of potential seabird prey (for, glaciers undergo melting: Rignot et al. 2003) and e.g. common tern Sterna hirundo Linnaeus, 1758: wind-driven land degradation processes (e.g. del Bugoni & Vooren 2004), such as small pelagic fish, Valle et al. 2010) following the clearance of natural especially orangespot sardine (Sardinella brasiliensis vegetation in Northeastern Patagonia (Pezzola et al. (Steindachner, 1879)) and anchovy, pelagic juvenile 2004). Differences in primary productivity can stages of demersal fish species and flying fish change the zooplankton distribution, as can tem- Cypselurus sp. (for, e.g. Cory’s shearwater: Bugoni perature changes (Spinelli 2012), for example by an et al. 2010). The slope, between 400 and 900 m influence on the relative abundance of copepods and deep, harbours vast and continuous deep-sea coral appendicularians. In one reported instance, massive reefs. The region is also home to more than 30 blooms of gelatinous zooplankton occurred when the species of cephalopods (Haimovici & Perez 1991), water temperature rose by 28C, rendering the tidal which are important in seabird diet (e.g. Magellanic fronts off Patagonia less prominent and depressing penguins: Fonseca et al. 2001; Pinto et al. 2007; copepod populations (Sabatini & Martos 2002). Baldassin et al. 2010; albatrosses and shearwaters: Much work remains to be done in order to under- Santos & Haimovici 2002; Petry et al. 2007, 2008, stand bottom-up effects in this ecosystem, and put 2009; southern fulmar: Fonseca & Petry 2007; them into perspective with top-down effects due to southern giant petrels (Macronectes giganteus (Gme- the massive fisheries. lin, 1789)): Petry et al. 2010). Migratory species such as Argentine shortfin squid (Illex argentinus (Castellanos, 1960)) use the South Brazil Shelf as a South Brazil Shelf LME spawning and nursery ground in winter (JuneÁ The South Brazil Shelf LME extends from central September), while spending the summer in the Brazil (228S) to Uruguay (348S, Figure 1), and has a colder waters of the Patagonian Shelf (Perez et al. wide shelf, extending up to 220 km (Sherman & 2009), utilizing the Brazil and Falkland/Malvinas Hempel 2009). The oceanography of the South Currents for long-distance transport. Brazil Shelf LME is complex. It is influenced by Breeding seabirds on coastal islands and sandy the oligotrophic, southward-flowing Brazil Current, beaches (Figure 4; Antas 1991) include brown by two sources of nutrient-rich Sub-Antarctic water boobies (Sula leucogaster (Boddaert, 1783)), neotro- (the Falkland/Malvinas Current and the South pic cormorants, magnificent frigatebirds (Fregata Atlantic Central Water) and by estuarine outflows. magnificens Mathews, 1914), kelp gulls (Larus Seasonal variability in the southern part of the dominicanus Lichtenstein, 1823), brown-hooded LME depends on seasonal migration of the BrazilÁ gulls (L. maculipennis Lichtenstein, 1823), snowy- Malvinas Confluence region. This confluence, also crowned tern (Sterna trudeaui Audubon, 1838), termed the Subtropical Convergence, shows a typi- South American terns (S. hirundinacea Lesson, cal northern limit around 308S in winter (reaching 1831), Cabbot’s tern (Thalasseus acuflavidus (Cabot the South Brazil Shelf LME) and 468S in summer 1847)) and royal tern (Thalasseus maximus (Bod- (in the Patagonian Shelf LME: Ciotti et al. 1995). daert, 1783)). Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 The Sub-Antarctic waters and northward extensions Although Procellariiformes do not breed in the of the La Plata River plume cause peaks in chlor- South Brazil Shelf LME, the region provides im- ophyll and primary production in winter (AugustÁ portant foraging grounds for Procellariiformes such September) in the southern part of the South Brazil as wandering albatross, Tristan albatross (Diomedea Shelf LME (Garcia et al. 2004). However, another dabbenena Mathews, 1929), black-browed albatross, source of productivity acts in the austral summer, as northern royal albatross, southern royal albatross the shelf edge and wind-driven upwellings of nu- (D. epomophora Lesson, 1825) and shy-type albatross trient-rich waters are intensified by the trade winds, (Thalassarche cauta/steadi), Atlantic yellow-nosed and the overall productivity in the LME is thus albatross (T. chlororhynchos (Gmelin, 1789)), spec- higher in summer. tacled petrel (Procellaria conspicillata Gould, 1844), Furthermore, large coastal lagoons and wetlands white-chinned petrel, Cape petrel, southern ful- such as the Patos/Mirim Lagoon system support a mars, great shearwaters, sooty shearwater, Manx very rich biodiversity, and the freshwater outflow is shearwaters, Cory’s shearwaters and Wilson’s storm an important source of nutrients for the shelf waters petrels (e.g. Neves et al. 2006; Bugoni et al. 2008b). (Ciotti et al. 1995). Ring recoveries have indicated that seabirds reach This LME provides important reproduction and the area for the non-breeding season from places feeding grounds for pelagic and demersal fish, such as the British Isles, Iceland, Finland and North 348 P. Quillfeldt and J. F. Masello

Figure 4. South Brazil Shelf LME seabirds: spectacled petrel (upper left), juvenile black-browed albatross (upper right), Atlantic yellow- nosed albatross (lower left) and a mixed group of royal terns, Cabbot’s tern, and snowy-crowned tern in breeding plumage, with non- breeding South American terns (lower right). Photographer: Leandro Bugoni.

America in the Northern Hemisphere, as well as Tedeschi 2009). Warm episodes of ENSO in the from southern breeding sites such as New Zealand, Pacific cause abundant rainfall in southern Brazil, South Georgia, South Orkneys and Tristan da Uruguay and northeastern Argentina, mainly due to Cunha (Olmos 2002). Magellanic penguins migrate an increased frequency of extreme rainfall events north from their breeding sites in Patagonia, many of (e.g. Ropelewski & Halpert 1987, 1989; Grimm & them reaching up to Uruguay and Brazil (Boersma Tedeschi 2009). Thus, in El Nin˜o years, the fresh- et al. 1990), which is also important for juveniles water outflow is greater and the productivity is

Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 (Garc´ıa-Borboroglu et al. 2006). Olrog’s Gull (Larus enhanced. For example, the high precipitation in atlanticus Olrog, 1958), royal and Cabbot’s terns also the El Ninõ spring 1977 resulted in nutrient-rich migrate north, reaching the coasts of Uruguay and Coastal Water (i.e. the waters formed by freshwater even Brazil (Escalante 1984; Collar et al. 1992; outflow) extending over the entire shelf from Uru- Bugoni & Vooren 2005). guay at 368S to north of Rio Grande at 328S, and The variability of phytoplankton biomass in the in the El Ninõ spring 1987, Coastal Water occupied South Brazil Shelf LME has been related to the a large extension over the shelf reaching 130 km seasonal latitudinal displacement of the Subtropical offshore near 338S, compared with only 20Á30 km in Convergence and to the freshwater outflow of La 1988 (Ciotti et al. 1995). Apart from nutrient input Plata River and Patos Lagoon. As the amount of by freshwater, the El Ninõ events influence wind chlorophyll in shelf waters is related to nutrients patterns. Cold (warm) SST anomalies in the tropical supplied by the freshwater outflow, strong inter- Pacific Ocean are associated with an intensification annual variability in line with the ENSO conditions of the southeasterlies (northwesterlies) over the Rio is observed (Ciotti et al. 1995; Garcia & Garcia de la Plata Estuary (Simionato et al. 2005). Thus, 2008), due to the relationship between precipitation ENSO events have an important impact on the rates in southern Brazil and the ENSO cycle (e.g. variability of phytoplankton production in the south- Ropelewski & Halpert 1987; Kane 2002; Grimm & ern Brazilian coastal areas, and the magnitude of the Impacts of climate variation on South American seabirds 349

La Plata impact on the southern Brazil Shelf (north propose two possible mechanisms: an increase in of the river mouth) can show high interannual storms, or poor food availability. Penguin carcasses variations, depending on the combined (sometimes appear on Brazilian beaches after strong storms. opposing) effects of both alongshore wind stress and Studies suggest that storms may be coupled to magnitude of river discharge (Garcia & Garcia 2008). ENSO and increases in frequency in the area (e.g. Variability is also caused by differences in the Escobar et al. 2004; D’Onofrio et al. 2008). In prominence of Sub-Antarctic waters. For example, March 2004 the first ever reported hurricane in the onshore (southeasterly) winds can cause a greater South Atlantic hit southern Brazil and displaced dominance of Sub-Antarctic waters over the shelf. Atlantic petrels (Pterodroma incerta (Schlegel, 1863)) On the other hand, northwesterly offshore winds and inland, up to 420 km from the coast and 1100 m consequent offshore transport following periods of above sea level (Bugoni et al. 2007). On the other high precipitation during El Ninõ conditions can hand, poor food availability for the penguins may be cause upwelling of deeper waters, rich in nutrients, the result of current displacement, in particular in to the euphotic zone on the mid shelf (Ciotti et al. conditions when the warm and oligotrophic waters 1995). Cold SST anomalies may be related to of the Brazil Current prevail at the southern Brazi- ENSO events (Lentini et al. 2001). In particular, lian coasts and displace the colder Falkland/Mal- anomalous cold (warm) waters occur via northward- vinas waters southwards (Ma¨der et al. 2010). propagating anomalies generally in every warm In summary, it seems crucial to study the inter- (cold) ENSO1 year in the present climatology annual variability in seabird abundance in this (Lentini et al. 2001). These events can radically globally important wintering area, ideally in connec- change the local ecosystem dynamics. For instance, tion with studies using dataloggers to follow indivi- recruitment failures of the Brazilian sardine may be dual birds. Due to the very different requirements of linked to the occurrence of cold or warm SST the species, any effects of climate change on seabirds anomalies (Lentini et al. 2001). in the South Brazil LME would be expected to affect Furthermore, with freshwater and SST, an in- birds with cold-water preference differently to those crease in red tide occurrences with climate change with a warm-water preference. (e.g. Edwards et al. 2006) might be relevant for seabirds. Dinoflagellate dominance causing red tides (harmful algal blooms) is a recurring phenomenon Summary and research priorities along the southern Brazilian and Uruguayan coasts Overall, seabird responses to climatic variability that seems to be related to the oceanographic suggest that many seabirds will be vulnerable to at conditions offshore. In 1993, massive mortality of least some of the environmental changes affecting intertidal benthic fauna was related to the accumula- South American waters due to anthropogenic cli- tion of dinoflagellates in the surf zone, due to the mate change (Table II). While several studies have action of onshore winds (Odebrecht et al. 1995). considered the effects of global climatic cycles, like Despite a rich literature on environmental varia- ENSO, on seabird populations in South America, bility in the region, there are very few studies on the only a few long-term studies have investigated the responses of seabirds to environmental conditions in effects of global warming in South American sea- this LME. Different habitat preferences were found birds. Seabird conservationists have not seen climate Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 in two closely related Procellaria petrels (Bugoni et al. change as the most immediate threat, and uncer- 2009). While spectacled petrels prefer warm, off- tainties in future climates and their consequences are shore and mesotrophic or oligotrophic waters of the high in marine environments. Enough is known, southwest Atlantic Ocean, coastal cold and produc- however, to suggest that the impacts could be severe. tive waters are used extensively by wintering white- Accordingly, a comprehensive review on seabird chinned petrels (Phillips et al. 2006), but were conservation concludes that enhanced research is avoided by spectacled petrels (Bugoni et al. 2009). desirable on the potential effects on seabirds of Studies such as this should be followed up over climate change (e.g. Croxall et al. 2012). In parti- several years to link with environmental variability cular, the authors emphasized a need to identify the and, more importantly, with global climate change. seabird species and populations that are likely to be Ma¨der et al. (2010) observed that the years with most susceptible to sea-level rise as a more immedi- highest numbers of carcasses of Magellanic penguins ate threat, and pointed out that a better under- washed up on southern Brazilian coasts were years of standing of the effects of major shifts in ocean outstanding ocean climate, with either ‘El Ninõ’ or conditions on seabirds might assist in developing ‘La Ninã’ phenomena. Together with oiling, the management actions (e.g. Croxall et al. 2012). ENSO index explained 35% of the annual variation Long-term monitoring is needed to understand in Magellanic penguin mortality. Ma¨der et al. (2010) these connections between climate and the population 350 P. Quillfeldt and J. F. Masello

Table II. Overview of the seabird associations, proposed climatic trends and seabirds’ responses of the LME treated in detail in this review. The number of seabird species correspond to species whose distribution at sea overlaps with each Large Marine Ecosystem, as given by Croxall et al. (2012, supplement, table S3).

Number of seabird species and Climatic factors that may influence Evidence for climatic LME examples seabirds influences

Humboldt 105 species Strong seasonal, interannual and Seabird breeding failures and Current longer-term variability, periodic emigration during strong El Nin˜o LME Breeding/resident: occurrence of ENSO, leading to events well documented, otherwise Humboldt penguin, sooty shearwater, very variable productivity climate influences little known wedge-rumped storm-petrel, Elliot’s storm petrel, Markham’s storm petrel, Models forecast reduced Eastern Peruvian diving petrel, Peruvian pelican, Pacific ENSO activity, in line with Peruvian booby, guanay cormorant, recent cooling trend Peruvian tern, Inca tern, band-tailed gull, grey gull

Non-breeding/wintering: black-browed albatross, Salvin’s albatross, white-chinned petrel, Juan Fernandez petrel, thin-billed prion, blue-footed booby, red phalarope, Franklin’s gull Patagonian 73 species No clear trends proposed, possibly SST anomalies affect seabird Shelf LME LME is affected by a poleward provisioning (e.g. thin-billed prion) Breeding/resident: shift in the maximum wind zone and survival (rockhopper penguin, black-browed albatross, Wilson’s storm associated with the circumpolar gentoo penguin) petrel, thin-billed prion, common diving westerlies and an increase in petrel, Magellanic diving petrel, southern productivity Severe rains frequently cause breeding rockhopper penguin, gentoo penguin, failures (Magellanic penguin, southern Magellanic penguin, kelp gull, imperial rockhopper penguin, black-browed shag, rock shag, dolphin gull, South albatross) American tern

Non-breeding/wintering: wandering albatross, grey-headed albatross, light-mantled albatross, white- chinned petrel, Wilson’s storm petrel, great shearwater, Manx shearwater, Cory’s shearwater, Arctic tern

South Brazil 51 species Southern Shelf: in El Nin˜o years, the Climate influences little known, few Shelf LME freshwater outflow is greater and the case studies: e.g., ENSO anomalies Breeding/resident: productivity is enhanced related to Magellanic penguin brown booby, neotropic cormorant, mortality magnificent frigatebird, kelp gull, brown- South Brazil Bight and Eastern hooded gull, snowy-crowned tern, South slope: stronger upwelling in El Nin˜o

Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 American tern, Cabbot’s tern, royal tern years, resulting in more productive Sub-Antarctic water Non-breeding/wintering: wandering albatross, Tristan albatross, black-browed albatross, northern royal albatross, southern royal albatross, shy- type albatross, Atlantic yellow-nosed albatross, spectacled petrel, white-chinned petrel, Cape petrel, southern fulmar, great shearwater, sooty shearwater, Manx shearwater, Cory’s shearwater, Wilson’s storm petrel, Magellanic Penguin

dynamics of seabirds. Long-term studies with indivi- few species and sites around South America, hopefully dually known animals would be particularly desirable, more data sets from previous multi-year research and as they allow for detecting and understanding the data from reports can be compiled. A retrospective temporal trends in life-history traits and to estimate analysis of guanay cormorant and Peruvian booby the inheritability of life-history traits (e.g. Visser population numbers (Jahncke et al. 2004) shows that 2008). Although long-term data sets only exist for a such data, combined with data from fisheries landings Impacts of climate variation on South American seabirds 351

and environmental proxies, can be used to reconstruct et al. 2002; deYoung et al. 2004; Richardson & the mechanisms governing seabird dynamics. About Schoeman 2004; Hays et al. 2005). Over 90 years, 94% of the variation in seabird numbers from 1925 the timing of annual migration of squid and fish to 2000 were explained by two factors governing followed decadal trends in ocean temperature, being primary production in the Humboldt upwelling sys- later in cool decades and up to 1Á2 months earlier in tem, namely wind stress and sea-surface temperature, warm years (Southward et al. 2005). Some copepod and the competitive effect of the fishery that limits communities have shifted as much as 1000 km prey availability (Jahncke et al. 2004). northward (Beaugrand et al. 2002). Seabird species Our understanding of the processes would also with a rather fixed timing of breeding or prey choice benefit from more coordinated research efforts. For would be expected to experience such decoupling example, Peruvian boobies have been studied in from the peaks of food availability. The combined Peru (Jahncke et al. 1997; Jahncke & Goya 1997, impact of bottom-up effects due to climate change 2000; Zavalaga et al. 2010) where their distribution and top-down effects due to fisheries further merits at sea is strongly correlated with the distribution of attention. On the other hand, as dataloggers become their near-exclusive prey, anchovies (Jahncke et al. 1998). In northern Chile, in contrast, the diet has ever smaller, seabird-deployed dataloggers might be been found to be more variable (Ludynia et al. used to supplement the study of marine environ- 2010), but it remains unclear whether the observed mental variables (e.g. Wilson et al. 2002, 2007). differences reflect differences among years or sites. In an advanced stage, these data can be combined Some previous studies also have shown a great with future climate scenarios for marine habitats. potential to reflect environmental variability. For Thus, species distribution models (i.e. spatially example, a study of the weight of dark-rumped petrel explicit habitat modelling applied to data obtained (Pterodroma phaeopygia (Salvin, 1876)) chicks in the from biotelemetry) based on current ecological niche Galapagos Archipelago has been conducted in 1981Á constraints can be used to project future species 1985, showing high variability (e.g. at age 45 days distributions and predict seabird responses to top- chicks weighed 290969 g during the 1983 El Nin˜o, down and bottom-up food web changes. Such compared with 415952 g in 1981, 1984 and 1985: models would ideally be refined with data on Ainley et al. 1988). Studies such as this should be phenotypic plasticity within seabird spatial responses continued in combination with modern biotelemetry to climate change (e.g. Gre´millet & Boulinier 2009; methods, such as miniature GPS and geolocation Lescroe¨l et al. 2010). loggers to follow the at-sea distribution and with diet More detailed information on the responses of analyses. seabirds to climate variability and climate change The challenge is further to join forces with marine will finally enable wildlife managers to plan measures biologists working on lower trophic levels and for assisting seabirds to adapt to climate change (e.g. increase joint systematic sampling efforts, in order Chambers et al. 2011), for example by informed to detect functional links between seabird and prey decisions to define marine protected areas and to dynamics and distribution. For example, climate regulate fisheries (e.g. Gre´millet & Boulinier 2009). change can lead to decoupling of phenological relationships (also termed matchÁmismatch: Cushing Downloaded by [Petra Quillfeldt] at 07:08 25 February 2013 1990), with important ramifications for trophic in- Acknowledgements teractions, including altered food-web structures and eventually ecosystem-level changes (e.g. Edwards & PQ was supported by grants provided by the Richardson 2004). A climate-forced seasonal mis- Deutsche Forschungsgemeinschaft DFG (Qu 148/ match between the hatching of seabird chicks and the 1ff). We would like to thank the editors and three availability of prey has been detected in zooplankti- anonymous referees for helpful comments on the vorous and piscivorous auks (Hipfner 2008; Watanuki manuscript. et al. 2009). 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