persistence of hotspots and variability of seabird species...

Persistence of hotspots and variability of seabird species richnessand abundance in the southern California Current

JARROD A. SANTORA1,2,� AND WILLIAM J. SYDEMAN

2

1Department of Applied Mathematics and Statistics, Center for Stock Assessment Research, University of California,110 Shaffer Road, Santa Cruz, California 95060 USA

2Farallon Institute for Advanced Ecosystem Research, 101 H Street, Suite Q, Petaluma, California 94952 USA

Citation: Santora, J. A., and W. J. Sydeman. 2015. Persistence of hotspots and variability of seabird species richness and

abundance in the southern California Current. Ecosphere 6(11):214. http://dx.doi.org/10.1890/ES14-00434.1

Abstract. Aggregations of seabirds at sea may provide information on centers of enhanced trophic

interactions and concentrating mechanisms, however, to date most studies lack quantification of

persistence, a key hotspot characteristic. Persistence statistics may reduce uncertainty about seabird

habitat use, improve understanding of the spatio-temporal scales of pelagic food web dynamics, and

inform conservation planning. Using 26 years (1987–2012, 47 surveys) of shipboard surveys from a 300K

km2 study area within the southern California Current Ecosystem, we conduct a spatial assessment of the

inter-annual and seasonal dynamics of the persistence of seabird hotspots and identify recurring sites of

elevated seabird species richness and abundance. Previous studies document declines in abundance, but

were based on broad spatial standardizations to assess where declines may have occurred. Here, we refine

the hypothesis that seabird populations have declined off southern California by focusing on persistently

used habitats in nearshore or offshore domains. We demonstrate that spatio-temporal variability of seabird

distribution and abundance is characterized by anomalous events embedded within trends. In addition to

identifying the locations of persistence of seabird aggregations, we found significant declines in species

richness and the density of sooty shearwater (Puffinus griseus) and Leach’s storm petrel (Oceanodroma

leucorhoa); in contrast, black-footed albatross (Phoebastria nigripes) abundance appear to be increasing. This

assessment provides a spatially-explicit framework for future evaluations of biophysical drivers of seabird

hotspots and their associations and impacts on forage fish and zooplankton populations.

Key words: albatross; CalCOFI; hotspot persistence; shearwater; spatial ecology; species richness; trend assessment.

Received 9 November 2014; revised 13 March 2015; accepted 9 June 2015; published 9 November 2015. Corresponding

Editor: C. Lepczyk.

Copyright: � 2015 Santora and Sydeman. This is an open-access article distributed under the terms of the Creative

Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided

the original author and source are credited. http://creativecommons.org/licenses/by/3.0/

� E-mail: [email protected]

INTRODUCTION

Seabird population and community dynamics

respond to local to large spatio-temporal scales in

marine ecosystems (e.g., fronts to ocean basins

and days to decades), such that their distribution

and abundance at sea can serve as indicators of

marine ecosystem variability (Veit et al. 1997,

Hyrenbach and Veit 2003, Ainley et al. 2009, Piatt

et al. 2007, Sydeman et al. 2009, 2015). Many

seabird species exhibit long-distance migrations

among disparate marine ecosystems and hemi-

spheres to feed on seasonally abundant forage

species (Veit et al. 1996, Shaffer et al. 2006), and

therefore may affect marine food webs regionally

and globally. Quantifying interannual spatial

variability of seabirds at sea also provides

valuable indicators of ecosystem health and

habitat quality (e.g., pollution), as well as

information on key scales of variability concern-

v www.esajournals.org 1 November 2015 v Volume 6(11) v Article 214

ing trophic interactions in pelagic ecosystems(Ainley et al. 2009, Sigler et al. 2012, Santora andVeit 2013). Quantifying the persistence of seabirdhotspots (i.e., the reoccurrence of locales of highabundance and/or diversity) may reduce uncer-tainty about seabird habitat requirements (e.g.,marine Important Bird Areas; Lascelles et al.2012), and facilitate future investigations ofseabird-forage interactions needed for improvingecosystem-based fishery management (Santora etal. 2014), yet is rarely accomplished. In this study,we use an extensive shipboard data set (26 years)to quantify persistence of seabird hotspots withinthe southern California Current Ecosystem (CCE;Fig. 1).

The California Cooperative Oceanic FisheriesInvestigations (CalCOFI) program maintains oneof the longest marine sampling programs in theworld, and since 1987 includes routine countingof seabird abundance (Veit et al. 1996, 1997,Hyrenbach and Veit 2003). The CalCOFI pro-gram has quantified the influence of climatestates on marine ecosystem functions (McGowanet al. 2003, Di Lorenzo et al. 2008), as well aslong-term trends in physical oceanographicfeatures (Bograd and Lynn, 2003, Bograd et al.2008) and populations of zooplankton (Roem-mich and McGowan 1995, McGowan et al.1998),larval fishes (Hsieh et al. 2009, Koslow et al.2011), and seabirds (Veit et al. 1997, Sydeman etal. 2015). Changes in oceanographic conditionsand key zooplankton and larval fish relate tochanges in seabird abundance (Sydeman et al.2015), but changes in distributional statistics andpotential trophic linkages between seabirds andtheir prey have yet to be examined. Therefore, anassessment of the spatio-temporal variability ofseabird population and community dynamicswill facilitate future spatial integration of theimportant CalCOFI data set (Fig. 1).

The assessment of seabird populations at sea isdependent on the size of an area surveyed andthe consistency and repeatability of surveysacross many years (Nur et al. 2011, Lascelles etal. 2012, Santora and Veit 2013). Seabirds tend toconcentrate in suitable foraging habitat; somespecies concentrate near the coast, whereasothers are more oceanic and found 500þkmoffshore (Hyrenbach and Veit 2003). Therefore,deriving simple means or total counts of seabirdsover a large survey area such as CalCOFI

(Sydeman et al. 2015) without adjusting forvariability in spatially referenced survey effortcan lead to an increase in uncertainty abouttrends in species populations. Here, we focus onthe spatio-temporal variability of seabirds andconduct an assessment of their inter-annual andseasonal dynamics, and apply an application forthe identification and location of persistentseabird species richness and abundance hotspots(i.e., reoccurring areas of high abundance andspecies; Suryan et al. 2012, Santora and Veit2013). With more than double the length (26years; 1987–2012) of previously published timeseries on individual species (Hyrenbach and Veit2003) we apply a spatial standardization (e.g.,grid-based approach) to investigate the hypoth-esis that seabird densities have declined in thesouthern CCE (Veit et al. 1997, Sydeman et al.2015). Specifically, we assess whether the spatio-temporal variability of seabirds is characterizedby anomalies (events; influxes of migrants), long-term trends or both. This assessment will benefitseabird conservation and marine spatial manage-ment of the CCE and will provide a spatiallyexplicit framework for future evaluation ofbiophysical drivers of seabird hotspots.

METHODS

Study areaThe CalCOFI sampling of the Southern Cal-

ifornia Bight includes 6 parallel survey lines (eastto west) that extend from the coast out to 470–700 km (northern most line is shorter) offshore(Fig. 1). The survey area covers approximately300,000 km2. The 2000 m isobath runs southeast(;1358) and represents a distinct change inbathymetry (e.g., Santa Rosa Ridge), movingfrom the coastal Channel Islands and deep basinsonshore to the abyssal plain offshore, which ispunctuated by the location of seamounts (Fig. 1).Four distinct hydrographic and biogeographicdomains have been described: (1) southerncoastal domain influenced by northward move-ment of warm waters from the subtropics, (2)northern coastal domains influenced by upwell-ing at Pt. Conception, (3) the transition (middle)domain associated with the generalized corelocation of the California Current, and (4) oceanic(outer) domain (Hayward and Venrick 1998; Fig.1). Jasper seamount, an underwater volcano with


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Fig. 1. (Top panel) The southern California Current region, CalCOFI survey domain and location of grid cells

used to assess seabird hotspots; dashed lines indicate the approximate boundaries separating the coastal basin,

middle and outer domains; GI¼Guadalupe Island, LA¼Los Angeles, SM¼ San Miguel Island, SR¼ Santa Rosa

Island, SCr ¼ Santa Cruz Island, SCa ¼ Santa Catalina Island, SCl ¼ San Clemente Island, SN ¼ San Nicholas

Island, SD ¼ San Diego. (Bottom left panel) Location of hydrographic and biological stations sampled during

CalCOFI (illustration purposes only) and (bottom middle and right panels) distribution visual survey effort for

seabirds during spring and summer CalCOFI surveys, 1987–2012. Contour lines are the 200 m, 1000 m and 2000

m isobaths.


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a summit depth of ;700 m is located in thesouthwest study region (;30.58 N, 123.48 W) andis likely an attractive area for top predators.Offshore of Point Sal and Point Conception(prominent headlands that influence upwellingand hydrographic variability), the southwardflowing California Current moves along the coastand also meanders offshore (via jets) where itmeets sub-tropical waters that are characteristicof the far western CalCOFI survey region(McClatchie 2013). At approximately 328 N, theCalifornia Current moves towards the east andforms the southern boundary of cyclonic gyreknown as the Southern California Eddy (Cher-eskin and Niiler 1994); a feature that influencesupwelling dynamics, including frontal develop-ment, within the onshore coastal domain. Com-paratively, the coastal domain has less shelfhabitat (indexed by the 200 m isobath contour)and upper slope depth (indexed by area withinthe 200–500 m isobaths) along the coast thanoffshore around the islands (McClatchie 2013;Fig. 1). Furthermore, the coastal domain containsnumerous deep basins, which adds to thebathymetric complexity and hydrographic circu-lation of the region.

Seabird surveys and species selectionThe methodology for counting seabirds on

CalCOFI surveys is detailed by Veit et al. (1996)and Hyrenbach and Veit (2003). Briefly, stan-dardized counts are conducted during daylighthours while the vessel was underway at speeds.5 knots between hydrographic sampling sta-tions. All seabirds sighted within a 300 m arcfrom the bow to 908 to the side with the bestvisibility (least glare) are identified to species andenumerated (Tasker et al. 1984). Survey effortand counts of seabirds are aggregated in 3 kmintervals and stored in a relational database

(http://sccoos.org/data/seabirds/). This study in-vestigates spring and summer CalCOFI surveys.Spring and summer surveys provide importantinformation due to seasonal upwelling (Checkleyand Barth 2009) as well as the presence ofmigrants in the system (Hyrenbach and Veit2003, Yen et al. 2006). The months of the springand summer surveys are March–April and July–August, respectively; 47 surveys were conductedover the years 1987–2012. We omitted the 1991survey from the spring survey list because itoccurred a month earlier (February) than themean spring start date (first week of April) and itshould probably be considered a winter survey.There were no seabird surveys conducted insummer 1994 and spring of 1997 and 2007. Therewas an error in the GPS assigned to the seabirddata logging computer and the coordinate datawere not available for the 2009 spring surveyresulting in this year being omitted from thissynthesis.

Species included in the species richness calcu-lations were predetermined by Appendix Aprovided by Hyrenbach and Veit (2003), whichincludes 68 species/taxa. For individual speciesassessments, we focused on the most numerousmigratory species encountered during spring andsummer CalCOFI surveys (Hyrenbach and Veit2003, Yen et al. 2006), including sooty and pink-footed shearwaters, Leach’s storm petrel (Ocean-odroma leucorhoa), Cook’s petrel and black-footedalbatross (Phoebastria nigripes). These species alsorepresent a variety of life history and feedingbehaviors, including trans-hemisphere migrants(shearwaters, Cook’s petrel), surface-feeding anddiving (Table 1). Furthermore, the InternationalUnion for the Conservation of Nature (IUCN;Rodrigues et al. 2006) classifies some of thesespecies as either near threatened and/or vulner-able (Table 1); assessing the persistence of

Table 1. Biological aspects and conservation status of species examined in this study; weight and feeding ecology

derived from Hyrenbach and Veit (2003). IUCN is International Union for Conservation of Nature; website

accessed on 9 March 2015.

Species Weight (g) Feeding method IUCN status IUCN population trend

Sooty shearwater (Puffinus griseus) 787 surface and diving near threatened decreasingPink-footed shearwater (Puffinus creatopus) 721 surface and diving vulnerable unknownLeach’s storm petrel (Oceanodroma leucorhoa) 39.8 surface least concern stableCook’s petrel (Pterodroma cookii ) 178.5 surface vulnerable increasingBlack-footed albatross (Phoebastria cookii ) 3148 surface near threatened increasing


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migratory species hotspots will provide geo-graphic reference points for their conservation.

AnalysisThe first objective of this study is to assess the

spatio-temporal persistence of seabird speciesrichness and abundance hotspots. The CalCOFIprogram samples a fixed grid of stations that ishighly replicated using consistent methodology(Bograd et al. 2003; Fig. 1). Integrating seabirdobservations with station data requires a grid-based approach to resolve spatially explicit timeseries that account for survey effort over time. Allshipboard tracklines, indexed by 3 km intervals(Yen et al. 2006; Fig. 1), was linked to a GIS, as wehave done for other studies in the CCE (Santoraet al. 2011a, b, 2012a, b). The extent of theshipboard trackline (total survey effort) andCalCOFI sampling stations determined the ex-tent and size of grid cells. This was accomplishedusing the create fishnet command in ArcView toproject the individual 3km sampling points ontoa grid with cells size of 0.78 3 0.78 (;4500 km2).The size of cells was chosen to account for totaltrackline effort (Fig. 1) and to reflect the layout ofthe CalCOFI hydrographic and biological sam-pling stations (Fig. 1) in order to permit futureintegration with those data sets. The grid processresolved the location of consistently sampledcells during 1987–2012 with 45 and 48 cells inspring and summer, respectively (Fig. 1).

We standardized sampling effort by assessingthe number of times the ship visited a cell and theamount of survey effort collected within that cell,relative to all cells in a given season over theentire length of the time series (Santora and Veit2013). To determine a threshold to use as a cutoff, we calculated the mean 6 SD of cell visitsand effort per season, then omitted all effort lessthan 1 SD below the mean. For spring surveys, itwas determined that a cell required at least 7visits for 24 km of survey effort; resulting in atotal of 573 cells visited, with a mean 6 SD of55.29 6 9.55 km per cell and total of 31,911 km.There was more effort during summer, so a cellrequired at least 9 visits for 24 km of surveyeffort; resulting in a total of 736 cells visited, witha mean 6 SD of 55.09 6 10.82 km per cell andtotal of 40,800 km.

We quantified the spatio-temporal mean, var-iance, anomaly and persistence of a cell’s value

for species richness as species per unit effort(SPUE) and abundance as individuals per uniteffort (IPUE; Santora and Veit 2013). For eachsurvey, rates of SPUE and IPUE are calculated bythe dividing the total number of species (out of68 species; Hyrenbach and Veit 2003) or individ-uals by the number of 3 km samples per cell. Forspatio-temporal comparison of SPUE and IPUEamong surveys, each survey and cell wasstandardized by subtracting its spatial meanand dividing by its standard deviation todetermine an overall time series for each surveyas well as a spatial anomaly per cell (computedfrom the grand spatial mean and standarddeviation). Moreover, we estimated the spatio-temporal persistence for SPUE and IPUE bycalculating the percentage of time a cell exhibiteda value that was greater than the grand spatialmean by 1 SD. We then mapped the spatialanomaly and persistence index per cell todetermine the location and persistence of SPUEand IPUE hotspots. Cells with higher percentagesare locations where SPUE and IPUE are persis-tently higher than the baseline standardizedanomaly and are considered hotspots. Formapping hotspots and to facilitate comparisonamong species, persistence is classified into 5classes using the Jenks natural breaks optimiza-tion method in ArcView; those cells greater than30% and 50% are considered medium and highhotspots, respectively; Santora and Veit (2013)describe all of these methods in greater detail.

The second objective is to determine trends inthe anomalies of seabird species richness andabundance based on habitat persistence data.This was accomplished by (1) fitting generalizedadditive models (GAM) to seabird anomalies forthe entire region, and (2) correlating (SpearmanRank) seabird anomalies within each grid cellover time and mapping significant (p , 0.05)correlations to reveal locations where trends areapparent. The GAM was fit to annual seabirdanomalies by including a smoothed term (spline)for year with a Gaussian link function (seabirdanomalies were normally distributed; J. Santora,unpublished data). Results of each GAM is plottedto describe the overall fit of the seabird anomalytime series for elucidating whether there aredeclines and/or periods of years with higheranomalies of particular species (i.e., events). AMonte-Carlo randomization procedure assesses


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the significance of spatial correlations (time serieswithin cells) for seabird anomalies. Locationswith significant (p , 0.05) correlations weremapped to provide additional context for under-standing change of seabird abundance withinparticular habitat and their potential associationwith bathymetric topographies (e.g., seamounts;Fig. 1).

RESULTS

Interannual and seasonal variabilityof species richness hotspots

The spatial anomaly and persistence of speciesrichness during spring and summer displayedcoherence in space and time, with higher valueslocated near the coast/islands and declining withincreasing distance offshore (Fig. 2). All persis-tent areas of species richness (.30%) werelocated near or shoreward of the 2000 m isobath.More high persistence cells (.50%) were foundduring spring (n¼ 9) than in summer (n¼ 6), andspring hotspots were broadly clustered along thecoast (Fig. 2). However, the spatial anomaly ofspecies richness during summer was clusteredand exhibited higher anomalies than springspatial anomalies (Fig. 2). In general, summer-time richness anomalies were positive during thebeginning of the time series (1987–1993) andwere generally negative from 1995 onwards,except for 2000, 2006 and 2012 (Fig. 2). Springanomalies tended to exhibit fluctuations withalternating years of positive and negative anom-alies (Fig. 2).

Interannual and seasonal variabilityof species abundance hotspots

The abundance of sooty shearwaters wasspatially clustered along the coast and aroundthe Channel Islands (Fig. 3). Interestingly, as thenumerically dominant species, sooty shearwatersdisplayed no persistent hotspots during spring(weak persistence of 15–30%) and only threemedium persistent hotspots during summer (E1,F2 and G2) located near Pt. Conception. Highspatial anomalies of shearwaters during springwere located in the northeastern portion of thestudy area near the Channel Islands and Pt.Conception. Compared to spring, there werecomparatively fewer areas of high spatial anom-alies during summer (Fig. 3). In both spring and

summer time series, the anomaly of shearwaterabundance was characterized by a relatively fewnumber of high positive anomalies at the start ofthe series; years 1987and 1990 during spring and1988 in summer (Fig. 3).

Compared to sooty shearwaters, pink-footedshearwaters (Fig. 4) displayed more medium andhigh persistence located during spring near theouter 2000 m isobath and within the central basinduring summer (Fig. 4); these areas are not sootyshearwater hotspots. Spatial anomalies of pink-footed shearwaters during spring occurred alongthe outer 2000 m isobaths near the ChannelIslands (cells E2, F3 and G3) and closer to shorenear Catalina Island (cells I3–4). Summer spatialanomalies of pink-footed shearwaters were lo-cated to the south of the Channel Islands (cellsG3–4) and to the east (cells H3 and I3; Fig. 4).The spring anomaly time series of pink-footedshearwaters displayed only one positive peakanomaly, during 2010 (Fig. 4). However, theirsummer temporal anomalies display substantialvariability with multiple positive peaks through-out the study period (Fig. 4), suggesting theiroccurrence during summer may relate to climateevents (e.g., ENSO).

Leach’s storm petrel displayed high spatialanomalies and persistent hotspots throughoutthe middle and outer domains (Fig. 5). Interest-ingly, there is an apparent geographic shift intheir distribution from spring to summer. Duringspring, high spatial anomalies and persistentcells are located to the west of 2000 m isobath,but during summer, spatial anomalies andpersistent hotspots are concentrated along the2000 m isobath (Fig. 5). Spring temporal anom-alies of Leach’s storm petrel are generallynegative with only a few positive years (Fig. 5),whereas the summer anomalies display a num-ber of consecutive positive years earlier in thetime series (Fig. 5).

Cook’s petrels are oceanic species and theirhigh spatial anomalies and hotspots are locatedin the outer domain (except for one spatialanomaly during summer that located off Pt.Conception; Fig. 6). During spring and summer,persistent hotspots (medium and high) for Cook’spetrels are found near and around Jasper’sSeamount (cell C4). The spring anomaly timeseries of Cook’s petrels exhibited only onepositive peak coinciding with the 1997 ENSO


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Fig. 2. Species richness: (A–D) spatial anomalies and persistence of hotspots and (E–F) standardized time series

(anomaly, mean and standard deviation) during spring and summer. Contour lines are the 1000 and 2000 m

isobaths.


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Fig. 3. Sooty shearwater: (A–D) spatial anomalies and persistence of hotspots and (E–F) standardized time

series (anomaly, mean and standard deviation) during spring and summer. Contour lines are the 1000 m and

2000 m isobaths.


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Fig. 4. Pink-footed shearwater: (A–D) spatial anomalies and persistence of hotspots and (E–F) standardized

time series (anomaly, mean and standard deviation) during spring and summer. Contour lines are the 1000 m and

2000 m isobaths.


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Fig. 5. Leach’s storm petrel: (A–D) spatial anomalies and persistence of hotspots and (E–F) standardized time

series (anomaly, mean and standard deviation) during spring and summer. Contour lines are the 1000 m and

2000 m isobaths.


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Fig. 6. Cook’s petrel: (A–D) spatial anomalies and persistence of hotspots and (E–F) standardized time series

(anomaly, mean and standard deviation) during spring and summer. Contour lines are the 1000 m and 2000 m

isobaths.


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event (Fig. 6), whereas during the summeranomaly time series, numerous positive peaksoccurred, some of which coincide with the 1992,1997 and 2009 ENSO events.

Black-footed albatrosses exhibit a greater num-ber of high spatial anomalies and persistenthotspots during spring compared to summer(Fig. 7). In general, highly persistent hotspots ofblack-footed albatross were more dispersedduring spring and more clustered during sum-mer within the outer domain (Fig. 7), possiblyindicating a redistribution pattern after the onsetof the spring upwelling transition. The anomalytime series of black-footed albatross duringspring displayed numerous positive peaks priorto 2002 and was generally negative afterwards.During summer, anomalies of black-footed alba-tross were generally negative up to 1999;afterwards they tended to be positive, suggestingan increase in their abundance.

Evaluation of trends in space and timeThe grand annual anomaly (computed over all

cells per season and year) of species richnessdisplayed a significant declining trend duringsummer (Figs. 8A and 9A), but not spring (notshown). Within the long-term trend, there isautocorrelation in the anomaly of summerspecies richness, with significant lags at 3–7years. There is no temporal autocorrelation inthe spring species richness. Relating changesover time within grid cells revealed specific areaswhere summer species richness significantlydeclined (Fig. 9A). For example, there are fourareas displaying significant declining trends inspecies richness: (1) cells off Pt. Conceptionextending outwards along the upwelling jet (cellsC2, D3, and E2), (2) central basin (cells G3–4), (3)middle domain (cells E5 and F5) and (4) thewarm oceanic region coinciding with the locationof and waters north of Jasper Seamount (cells B6,C6–7).

Of the five species analyzed, three (sootyshearwater, Leach’s storm petrel and black-footed albatross) exhibited trends in abundanceover time and space (Figs. 8 and 9). GAM fits toanomalies of seabird abundance were non-linearand suggest that temporal variability of thesespecies may be best characterized as a series ofautocorrelated years that are embedded withintrends over time. The anomaly of sooty shear-

water abundance decreased over time duringspring, but not summer (Fig. 8B). However, it isimportant to note 2 years (1987, 1990) at thebeginning of the spring time series should becharacterized as anomaly events and are likelyresponsible for decreasing linear trend. Spatially,significant declines in sooty shearwater abun-dance are located near Pt. Conception (F2), thecoastal basin (H4) and within the middle domain(F6) and outer domain near Jasper Seamount(C7; Fig. 9). The anomaly of Leach’s storm petrelabundance decreased during summer, but notspring (Fig. 8C). The GAM for Leach’s stormpetrel clearly shows several years (1990–1992)where abundance of this species was anomalous-ly high (Fig. 8C). Significant declines of stormpetrels are located throughout the outer domainwith a clustered distribution of cells located tothe north of Jasper Seamount (Fig. 9C). Stormpetrels also exhibited declines near the ChannelIslands (F3) and within the coastal basin (H4;same cell as sooty shearwater). In contrast, theanomaly of black footed albatross abundanceappeared to increase during summer (Fig. 8D).However, the fitted GAM for albatross clearlyshows that 1999–2003 was a sustained period ofanomalous albatross abundance; the highestanomaly occurs in 2012 and is likely influencingthe apparent increase (Fig. 8D). Significantincreases of albatross abundance are located inthe outer domain and near Jasper Seamount (Fig.8D).

DISCUSSION

Quantifying the spatio-temporal variability ofseabird distributions at sea by accounting forspatially explicit survey effort and habitat utili-zation, resolved persistent hotspots and trends inspecies richness and abundance. Analysis ofthese seabird time series provide evidence thatvariability of seabird densities at sea is bestcharacterized by years of autocorrelated condi-tions as well as lower frequency trends. Inparticular, we found a significant long-termdecline of species richness and confirmed thatthe abundances of sooty shearwater and Leach’sstorm petrel declined during spring and summer,respectively. In contrast, and somewhat surpris-ingly, abundance increases of black-footed alba-tross are apparent during summer within the


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Fig. 7. Black-footed albatross: (A–D) spatial anomalies and persistence of hotspots and (E–F) standardized time

series (anomaly, mean and standard deviation) during spring and summer. Contour lines are the 1000 and 2000

m isobaths.


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outer domain. All of these trends are specific toparticular areas and each requires further re-search to elucidate causal factors driving popu-lation change. In particular, we found declines inspecies richness and sooty shearwaters near Pt.Conception (an important upwelling zone andpreviously identified biological hotspot), so thebiophysical drivers of and trophic interactionswithin this hotspot require further study toelucidate possible mechanisms for the long-termchange. This study also highlights the impor-tance of Jasper Seamount in the offshore domainas a species richness and abundance hotspot.

Persistence of seabird hotspotsNo previous CalCOFI study conducted a

spatio-temporal assessment of seabird popula-tions at sea that accounts for the persistence ofspecies richness and abundance hotspots. Here,persistence indicates the probability of a hotspotreoccurring over 26 years, and the results of thissynthesis suggests some hotspots are clearlymore likely than others to persist between

seasons and among years. For example, speciesrichness hotspots exhibited some of the highestlevels of persistence (60–90%) and fidelity tocoastal locations. The described onshore tooffshore gradient in species richness hotspots islikely a relatively stable spatial aspect of theCalCOFI seabird data set due to bathymetry andpositioning of the California Current. Our resultsalso indicate that the persistence of abundancehotspots is dependent on season, whereby somespecies shifted geographically between springand summer. This may relate to migratorymovement patterns of bird species during springand redistribution of migratory species (e.g.,shearwaters) from southern to northern Califor-nia. Both sooty and pink-footed shearwatersdisplayed an increase in persistence and thenumber of hotspots between spring and summer,while sooty hotspots appeared to shift fromsouth to north (toward Pt. Conception), hotspotsof pink-footed shearwaters shifted in spring fromthe 2000 m isobath to shoreward around theChannel Islands. Leach’s storm petrel hotspots

Fig. 8. GAM fit to standardized anomaly time series of (A) summer species richness, (B) spring sooty

shearwater, (C) summer Leach’s storm petrel, and (D) summer black-footed albatross.


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are principally concentrated in the offshoredomain during spring, but strikingly, theirhotspots shifted toward the outer edge of the2000 m isobath during summer. Further researchshould assess the apparent shifts of these specieshotspots, and in particular, how persistence ofhotspots may relate to changes in ocean physicsand seasonal to longer-term availability of foragefish species.

Declines in species richness and abundanceWe have demonstrated that summertime spe-

cies richness has declined substantially over 26years and this clearly warrants further research.This corroborates the findings of Sydeman et al.(2009) in which we described initial trends inseabird richness and demonstrated declines maydepend on season. The decline of seabird speciesrichness adds to the collection of physical andbiological variables displaying long-term chang-es that collectively exemplify changes occurringwithin this marine ecosystem. Ocean warmingand shoaling of the oxygen minimum layer

(Bograd et al. 2003, 2008) have coincided withdeclines of mesopelagic fish (Hsieh et al. 2009,Koslow et al. 2011), and it now seems that theentire seabird community may be responding tovariability of forage fish populations (Sydeman etal. 2015). The decline of species richness ispuzzling, but may relate to either long-termclimate change in local breeding seabird popula-tions, and/or declines in populations that origi-nate outside of the CCE. In their comprehensiveanalysis of seabird time series from CalCOFIsurveys, Hyrenbach and Veit (2003) determinedthat variability of seabird community structurereflected years of warm and cool ocean temper-atures, with warmer years having higher num-bers of seabird species originating from theeastern tropical Pacific. Their study occurredfrom 1987 to 1998, a period now considered asgenerally warm (PDOþ) ocean conditions. Afterthe 1997/1998 El Nino event, conditions in theCCE during 1999 transitioned to La Nina (Bogradand Lynn 2001) and the following decade wascharacterized as an extended period of cool

Fig. 9. Locations where significant trends have occurred: (A) decline of summer species richness, (B) decline of

spring sooty shearwater, (C) decline of summer Leach’s storm petrel, and (D) increase of summer black-footed

albatross.


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ocean conditions (Bjorkstedt et al. 2010). There-fore, the decline in species richness could be dueto a decline in the number of seabird species withwarm water affinity that visit the southern CCE.For example, Leach’s storm petrel, the mostcommon pelagic bird in the middle and outerdomains, exhibited increases in their abundanceduring the warm decade (prior to 1999; Figs. 5and 9). As well, several other warm water affinityspecies, such as Cook’s petrel, pink-footedshearwater, black storm petrel (Oceanodromamelania) and Heerman’s gull (Larus hermanni )exhibited positive pulses in the southern CCEduring El Nino years (Veit et al. 1996, Hyrenbachand Veit, 2003). Since seabird community struc-ture relates to inter-decadal scale variability ofocean conditions, then perhaps the long-termdecline in species richness reported here, may infact indicate that ocean conditions within Cal-COFI study area are becoming less hospitable tomigrant seabirds. Nevertheless, the drastic de-cline in species richness reported here requiresfurther evaluation with respect to changes inphysical and biological conditions sampled bythe CalCOFI program.

Migratory seabird populations at sea exhibitlarge abundance fluctuations and most perceiveddeclines are either result of changes in spatialdistribution (i.e., shifts out of restricted samplingareas; Hyrenbach and Veit 2003), reflective ofocean conditions, or declines at breeding colonies(Ainley and Hyrenbach 2010). Substantial evi-dence exists for many species that suggestseabird populations have declined at breedingcolonies to threatened and endangered levels(Rodrigues et al. 2006). Populations of sootyshearwaters have declined at their breedingcolonies in New Zealand (Jones 2000, Scott etal. 2008), and it is likely that migrating popula-tions to the CCE should also reflect this decline.However, their interannual abundance off theU.S. West Coast is often highly variable in spaceand time (Briggs and Chu 1986, Veit et al. 1997,Santora et al. 2011a, Adams et al. 2012). It is alsoof concern that the early sooty shearwateranomalies in the CalCOFI time series may beattributed to a few observations of denseaggregations (shearwaters are gregarious andpatchy) within a coastal area that may have beeninfrequently surveyed. Furthermore, the lowspatio-temporal persistence of sooty shearwater

hotspots reported here likely indicates that high-density shearwater aggregations are spatiallyvariable. The GAM fit to the anomaly of sootyshearwater abundance suggests there is still anapparent decline during spring (no declineduring summer). Given the high variability andinfrequent strong anomalies that characterize thesooty shearwater time series, the significantdecline of sooty shearwaters may need furtherassessment with longer time series, and especial-ly from combining multiple observations collect-ed throughout the CCE (Veit et al. 1997, Adamset al. 2012).

Although Leach’s storm petrel displayed a fewsignificant declines at locations within the middleand outer domains (Fig. 9), the GAM fit to theiranomaly of abundance indicates this time seriescontains consecutive positive anomalies in theearly to mid-1990s with little variability to 2012.This result is consistent with the findings ofHyrenbach and Veit (2003), which stated thatanomaly of Leach’s storm petrel abundancerelates to warm ocean conditions and perhapsvariation in the flux of eastern tropical Pacificwater into the CalCOFI study area. By compar-ison, the anomaly of black-footed albatrossdisplayed significant increases over time in theouter and middle domains. The increases inalbatross abundance may indicate that theirpopulations are increasing (IUCN status; Table1) or that foraging conditions with the southernCCE are improving for albatross, and/or foragingconditions are less favorable in areas outside ofthe CalCOFI study area. Further research isrequired to elucidate the interactive effectsamong ocean conditions and forage species forexplaining variability and the apparent increasein albatross abundance.

Significance and future CalCOFI seabirdassessments

Resolving persistence of seabird hotspots isimportant for at least three reasons. First, from afood web perspective, biological hotspots inpelagic ecosystems are ecologically importantareas with high concentrations of marine specieswhere high rates of trophic transfer may occur(Nur et al. 2011, Santora et al. 2011b, 2012, Sigleret al. 2012); thus, their identification will advanceour understanding of how pelagic marine eco-systems are spatially organized. Moreover, little


SANTORA AND SYDEMAN

is known about species richness patterns inmarine ecosystems, so establishing where speciesrichness hotspots form and are maintained is ofgreat interest for advancing theory on howmarine systems are structured (Myers et al.2000, Worm et al. 2005, 2006). Second, migratoryseabirds are abundant members of the CCE andmay exert significant pressure on populations offorage species (Ainley and Hyrenbach 2010). Forexample, Chu (1984) estimated that 2 to 4 millionsooty shearwaters migrate to the CCE every yearand each individual requires 200–300 g of forage(fish, squid and krill) per day. A major objectiveof ecosystem-based fisheries management(EBFM) is balancing the dietary and consump-tion needs of seabirds while sustaining foragefisheries (Smith et al. 2011). Therefore, under-standing trophic interactions within persistentseabird hotspots could benefit EBFM and devel-opment of harvest rules for forage fisheries.Third, marine spatial management in the CCErequires information on the distribution andconnectivity of biological hotspots (Halpern etal. 2009, Nur et al. 2011, Santora et al. 2011b,Adams et al. 2012) in order to avoid potentialnegative interactions (e.g., seabirds and fishingvessels, oil spills; Hyrenbach et al. 2000, Hookerand Gerber 2004, Lascelles et al. 2012).

Our synthesis paves the way for integratedecosystem science aimed at understanding bio-physical processes and functional relationshipsamong trophic levels and future variability of theCCE. Quantifying biophysical drivers of seabird-forage hotspots will reduce uncertainty aboutnumerical responses between seabirds and for-age fish (Cury et al. 2011, Santora et al. 2014), andpromote identification of critical marine habitatimportant for sustaining seabird populations inthe CCE (Nur et al. 2011, Adams et al. 2012). Tothat end, numerical response models shouldcompare the spatio-temporal persistence of sea-bird hotspots to long-term changes in hydro-graphic conditions and forage fish abundance.Several locations exhibited long-term declines inspecies richness and abundance, but it is un-known how interactive changes in hydrographicconditions and forage species abundance mayhave varied within these areas of concern.Dynamic height in the CalCOFI area is importantvariable for predicting spawning locations offorage fish in the southern CCE (Asch and

Checkley 2013), and may relate to the persistenceof some seabird hotspots (Yen et al. 2006).Therefore, spatially-referenced numerical re-sponse models that combine ocean conditionsand forage fish, should help illuminate thedrivers of persistent hotspots (Santora et al.2014).

ACKNOWLEDGMENTS

Thanks to all CalCOFI seabird observers andRichard R. Veit and John A. McGowan for initiatingthe CalCOFI seabird program. Seabird surveys havebeen supported by variety of agencies and groups overthe years, including the National Science Foundation(California Current Ecosystem Long-term EcologicalResearch), NOAA (Integrated Ocean Observing Sys-tem via the Southern California Coastal OceanObserving System), the National Fish and WildlifeFoundation, David and Lucile Packard Foundation,the Moore family Foundation, and donors to theFarallon Institute. The NOAA-NMFS Integrated Eco-system Assessment program funded J. A. Santora forpreparation of this manuscript. W. J. Sydeman supportwas provided by NFWF and Farallon Institute. Thiswork was partially supported by the Center for StockAssessment Research (CSTAR), a partnership betweenthe Southwest Fisheries Science Center and theUniversity of California, Santa Cruz.

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