Relationship Among Prey Availability, Habitat, and the Foraging Behavior, Distribution, and Abundance of Common Terns Sterna Hirundo and Roseate Terns S. Dougallii

Vol. 506: 291–302, 2014 MARINE ECOLOGY PROGRESS SERIES Published June 23 doi: 10.3354/meps10834 Mar Ecol Prog Ser

Relationship among prey availability, habitat, and the foraging behavior, distribution, and abundance of common terns Sterna hirundo and roseate terns S. dougallii

Holly F. Goyert1,2,3,*

1Department of Biology, Doctoral Subprogram in Ecology, Evolutionary Biology and Behavior, The Graduate Center, City University of New York (CUNY), 365 Fifth Avenue, New York, NY 10016, USA 2College of Staten Island, CUNY, 6S-143, 2800 Victory Boulevard, Staten Island, NY 10314, USA

3Present address: Department of Forestry and Environmental Resources, Fisheries and Wildlife Program, Jordan Hall Addition 5215, North Carolina State University, Raleigh, NC 27695, USA

ABSTRACT: Analyses of the behavior, distribution, and abundance of seabirds tend to identify the importance of habitat variability and prey availability, yet ignore social facilitation. To quantify such influences on the foraging strategies of common terns Sterna hirundo and roseate terns S. dougallii, I implemented nonlinear density-surface models with distance sampling, using remotely-sensed habitat covariates. I collected tern and prey data aboard trawl surveys off the coast of Massachusetts, USA, selecting the 3 dominant regional prey categories: northern sandlance Ammodytes dubius, herring (Clupea spp., primarily Atlantic herring C. harengus), and anchovies (Anchoa spp.). The best models showed significant positive effects of tern flock size and variable sandlance abundance on common and roseate tern spatial patterns; additional predictors included herring abundance, relatively shallow water, high primary productivity, and intermediate sea surface temperatures. Furthermore, foraging roseate terns were associated with high sandlance abun dance. By establishing direct, positive relationships among terns, prey, and habitat, this study demonstrates how common and roseate terns act as community, fisheries, and ecological indicators. These 2 species evidently provide interspecific cues to the presence of prey; therefore, the conservation and management of roseate terns depends not only on the availability of sandlance and suitable habitat, but also on the ecology of common terns.

KEY WORDS: Social facilitation · Foraging strategy · Community ecology · Prey availability · Sand lance · Distance sampling · Distribution patterns · Spatial habitat models

Resale or republication not permitted without written consent of the publisher

INTRODUCTION impact prey availability, conventionally through bottom-up processes in the marine realm (Hunt & The direct effect of prey availability on the spatial Schneider 1987, Frederiksen et al. 2006, Grémillet et distribution and abundance of top marine predators al. 2008): habitat influences resource predictability, is difficult to quantify, and although essential for con- and this, in turn, drives interspecific differences in servation (Safina & Burger 1988, Diamond & Devlin prey utilization (Davoren et al. 2003, Weimerskirch 2003, Dänhardt & Becker 2011a), such information 2007, Elliott et al. 2009, Weimerskirch et al. 2010). remains sparse in the literature (Heinemann 1992, Seabirds are recognized as good ecological and Shealer & Kress 1994, Einoder 2009, Williams et al. fisheries indicator species, because they tend to be 2009). Behavioral and ecological factors together highly sensitive to habitat and prey patterns (Furness

*Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 292 Mar Ecol Prog Ser 506: 291–302, 2014

& Camphuysen 1997, Camphuysen & Webb 1999, ral & Saliva 2010), since the U.S. population of roseate Furness & Tasker 2000, Diamond & Devlin 2003, terns is federally ‘endangered’ and continues to de- Jaquemet et al. 2004, Le Corre & Jaquemet 2005, cline, whereas common terns have recovered since Jaquemet et al. 2007, Monticelli et al. 2007, Einoder the end of the 20th century millinery trade, and are 2009, Dänhardt & Becker 2011a). Still, little is under- listed as ‘special concern’ pursuant to the Massachu- stood about the trophic relationships involved in the setts Endangered Species Act (Mostello 2012). spatial patterns of habitat, prey, and top marine pred- The objective of this study was to evaluate poten- ators, which largely reflects the practical difficulties of tial drivers of the behavior, distribution, and abun- at-sea sampling. For example, sandlance (Ammodytes dance of common and roseate terns at sea, pre- and/ spp.) are very important prey to many seabird species or post-breeding, and to assess the extent to which in the Northwest Atlantic Ocean, particularly roseate prey availability, habitat variability, and social inter- terns Sterna dougallii and common terns S. hirundo actions predict interspecific similarities and differ- (Safina et al. 1990, Heinemann 1992, Gochfeld et al. ences in their spatial foraging patterns. I hypothe- 1998, Nisbet 2002, Rock et al. 2007), yet these forage sized that common and roseate terns associate with fish are notoriously difficult to sample, due to their each other and productive habitat in the search for slender body shape, burrowing habits, and irregular selected prey species, where sandlance largely distribution in the water column (Robards et al. 2000, determines the foraging behavior and ecology of the Dänhardt et al. 2011). Also, it is well documented at highly specialized roseate tern. To assess the ecolog- tern breeding grounds in the state of Massachusetts ical context of such trophic interactions between (MA), USA, that northern sandlance A. dubius, her- terns and their prey, I used shipboard survey data on ring (Clupea spp., primarily Atlantic herring C. haren- the distribution and abundance of selected seabirds gus), and anchovies (Anchoa spp.) are the dominant 3 and fish species, along with standard remotely sen- prey items delivered to common and roseate tern sed oceanographic parameters, viz. sea surface tem- chicks (Kirkham 1986, Safina et al. 1990, Tims et al. perature (SST) and chlorophyll concentration, an 2004, author’s unpubl. data). Yet, poor coverage of index of primary productivity (Amorim et al. 2009). terns at sea has kept biologists from uncovering how My analysis involved behavioral statistics and pre- the spatial distribution of terns links to the abundance dictive models with distance sampling, to evaluate of these prey. Sandlance, sea herring, and anchovies how tern foraging behavior and ecology respond to are neritic or epipelagic baitfish that experience short habitat, forage fish, and flocks of other common or (inter annual) and long-term (decadal) fluctuations in roseate terns, at sea. their distribution and abundance, resulting from consumptive impacts, fisheries pressure, and climate change (Overholtz et al. 2000, Overholtz & Link 2007, MATERIALS AND METHODS Lucey & Nye 2010, Nye et al. 2013); however, only At- lantic herring is commercially regulated. Common Data collection and roseate terns are susceptible to prey limitation (Safina et al. 1988), although roseate terns are poten- The North American breeding population of tially more vulnerable to fluctuations in sandlance roseate terns is divided amongst a few islands that availability, given that they are feeding specialists support a dominant proportion of the continental sub- (Gochfeld et al. 1998) that exhibit high foraging site fi- species Sterna dougallii dougallii (Gochfeld et al. delity (Heinemann 1992) and have better breeding 1998). Three of their largest breeding colonies in the success during years of high sandlance abundance northeastern US are shared with common terns and (author’s unpubl. data). Common terns, on the other are located in Buzzards Bay, MA, on Bird, Ram, and hand, are opportunistic generalists (Nisbet 2002) that Penikese Islands (see Fig. S1 in the Supplement may be more resilient to prey instability, through the at www.int-res.com/articles/suppl/m506p291_supp. use of local enhancement (Erwin 1977, author’s un- pdf). The breeding season generally runs from June publ. data). Local enhancement is a type of social fa- to July, although terns frequent the waters surround- cilitation, where individuals are drawn towards the ing Cape Cod, MA, from post- to pre-migration, in feeding cues issued by neighbors, as a way to exploit May to September. Throughout this study region, the unpredictable prey patches (Davo ren et al. 2003). Massachusetts Division of Marine Fisheries Identifying differences in the foraging strategies of (MADMF) provides one of the only long-term data - common and roseate terns, with respect to prey and sets available on fish abundance by season. Their Re- habitat selection, is a high conservation priority (Ama- source Assessment Bottom Trawl Surveys use sys- Goyert: Tern foraging: habitat, prey, and interspecies associations 293

tematic methods to provide an index of relative prey striped anchovy A. hepsetus, along with rainbow availability from sampled fish numbers (Garrison et smelt Osmerus mordax, which made up <1% of this al. 2002, King et al. 2010, Dänhardt & Becker 2011b, category, but was included to account for possible Nye et al. 2013). Shipboard surveys are valuable re- misidentification as anchovy during tern colony- sources in assessing animal movement patterns, be- based provisioning studies (author’s unpubl. data). cause they provide con tinuous data on real-time in- To access marine habitat data, I downloaded raster teractions among terns, other marine predators, and layers into ArcGIS: (1) 30 m bathymetry for MA and their prey, as gauged by their offshore behaviors, adjacent federal waters from the online Office of numbers, locations, and habitats (Camphuysen & Geographic Information (MassGIS), and (2) remotely- Garthe 2004, Camphuysen et al. 2004). I joined the sensed data from the National Aeronautics and MADMF cruise, aboard the National Oceanic and At- Space Administration’s (NASA) Aqua satellite using mospheric Administration’s (NOAA) RV ‘Gloria Duke’s Marine Geospatial Ecology Tools (Roberts et Michelle,’ for a period of 21 sampling days: 13 to al. 2010): 4 km monthly daytime SST (JPL PO.DAAC 18 May and 17 to 23 September 2010, and 11 to MODIS Global Level 3) and chlorophyll a (chl a; 20 May 2011. Trawls were conducted from dawn to GSFC OceanColor Level 3 Standard Mapped dusk, during which I continuously recorded data on Image). These covariates made up 8 data layers: (1) all observed species and behaviors while in transit depth (m); (2) SST (°C); (3) chl a concentration (‘Chl’, (stations were located up to 3 h apart). I followed es- mg m−3); counts at length of (4) sandlance (‘Sl’), (5) tablished protocols from offshore surveys (Goyert et herring (‘Hg’), and (6) anchovy (‘An’); and total num- al. 2014), using dis tance sampling along line transects ber of (7) common and mixed terns (‘CMT’) or (8) but resorting to 300 m strip transects during occa- roseate and mixed terns (‘RMT’): ‘mixed’ refers to sional bursts of high densities (Tasker et al. 1984, mixed species flocks of common and roseate terns Thomas et al. 2010). I used binoculars and entered that were difficult to distinguish at farther distance data directly into a computer using dLOG3 (R.G. Ford (e.g. 500 m). CMT and RMT are mutually exclusive Consulting), recording the bearing and distance of as covariates (depending on which species is treated observations using a range finder, with distance as a response variable); therefore, only 7 covariates bands calculated based on the geometry of observer could be analyzed at one time. height above the water (Heinemann 1981). The most suitable spatial scale for analysis fit the Two outside sources supplemented my seabird following criteria: large enough to accommodate observation data: (1) bottom trawl catch results, and autocorrelation (due to continuous tern sampling) (2) online geographic information system (GIS) mar- and to minimize the number of covariate cells with ine data layers. NOAA and MADMF employees missing data (attributable to discrete prey sampling), deployed an otter trawl net at stations that were ran- yet small enough to prevent diluting predictions with domly stratified by region and depth in MA state missing data, for example by projecting onto land. waters: each tow was standardized to 20 min at The spatial dispersion of bottom trawl stations 2.5 knots (King et al. 2010). I selected a subset of largely determined the optimal resolution: 15 km × these data to represent the dominant categories of 15 km raster cells (225 km2). Therefore, I aggregated fish species, by composition and size, delivered to covariate values by mean (depth, SST, chlorophyll, tern chicks in MA for those same years (2010−2011, number of fish by species), and tern abundance by author’s unpubl. data). By focusing on the distribu- sum, into this grid resolution. The total study area tion of sandlance, herring, and anchovy numbers, no (6750 km2) was made up of 30 cells, but data cover- longer than 15 cm, I evaluated whether the foraging age varied slightly by parameter and survey. I calcu- patterns of pre- and post-breeding adults (May or lated the length of track lines within each cell to September) overlap spatially with the distribution determine transect effort. Due to the size of these and abundance of those same prey species that they grid cells, the 3 largest shared MA breeding colonies feed to chicks (in June and July). The 3 fish cate- of common and roseate terns in the study area occu- gories included the following species, in order of pied neighboring grid cells (Fig. S1). decreasing biomass: (1) sandlance: northern sandlance; (2) herring: Atlantic herring, alewife Alosa pseudoharengus, blueback herring A. aestivalis, Data analysis American shad A. sapidissima, and Atlantic men- haden Brevoortia tyrannus (negligible in biomass); Distance sampling computes the detection proba- (3) anchovy: bay anchovy Anchoa mitchilli and bility of study subjects from their observed range 294 Mar Ecol Prog Ser 506: 291–302, 2014

(perpendicular distance to a line transect), for selected those with the lowest Akaike’s information the purpose of evaluating population abundance criterion (AIC) scores (Wood 2006, Zuur et al. 2012). (Thomas et al. 2010, Gjerdrum et al. 2012). Density- There was no need to account for autocorrelation in surface modeling (DSM, Miller et al. 2013a) imple- the models, since the 15 km grid scale properly ments distance sampling to determine the relation- accommodated for spatial autocorrelation, rendering ship among the spatial distribution of population it insignificant; Moran’s I values were computed abundance and covariates. I used the package ‘dsm’ with the midpoint coordinates of each cell using (Miller et al. 2013b) in R (R Development Core Team package ‘ncf’ (Bjornstad 2009). 2012), which integrates 2 components (a 2-stage Density-surface models were developed to esti- approach) to model the effect of habitat covariates on mate the distribution and abundance of all observed the distribution and abundance of terns. First, DSM common and roseate terns, irrespective of behavior. relies on the package ‘Distance’ (Miller 2012) to per- Therefore, to determine the effect of sampled prey form conventional distance sampling (CDS), or alter- numbers on the comparative behavior of each tern natively, with the addition of 1 covariate (visibility), species in the spring, I classified behaviors into ‘for- multiple covariate distance sampling (MCDS): these aging’ (milling or feeding, i.e. plunge-diving) and analysis engines fit a detection function (Fig. S2 in ‘not foraging’ (traveling, resting), then used a the Supplement) onto the observed tern counts. The 2-factor analysis of variance (ANOVA) and Tukey’s detection probabilities (P) are then used to calculate multiple comparisons. abundance over the sampled area (N, Table S1 in the supplement), as well as estimated abundance over the entire study area. The second DSM component RESULTS runs a generalized additive model (GAM) on the sampled data cells (n, Table 1), fitting abundance (N, The generalized variance inflation factors (GVIFs, Table S1) to covariates; next, by projecting the re sults Zuur et al. 2010) of all covariates were <2, indica- over modified (mean) covariate values that span the ting negligible collinearity, to allow that all combi- entire study area (at an identical scale), the user may nations of explanatory variables be assessed in the predict population distribution and abundance (of models (Fig. S3 in the Supplement). The distribution terns, see Fig. 2). The benefit of this approach is that of the response variables (histograms in Fig. S3) it allows the user to consolidate many surveys into 1 illustrates that the Poisson and negative binomial set of spatially-explicit predictions. families were indeed more appropriate for analysis Model selection involved testing combinations of than a Gaussian curve. For the DSM, the study area a limited number of parameters (depending on the (and prediction grid) consisted of 30 data cells, but degrees of freedom in each GAM), given the 7 pos- the total number of sampled data cells (n, Table 1) sible covariates. I evaluated 4 model categories de - was <90 for all 3 surveys, and < 60 for the 2 spring fined by the response variable and number of sur- surveys, due to missing data (survey coverage or veys analyzed: (1) common, roseate, and mixed data availability). terns (‘CRMT’) over all 3 surveys (62 possible com- The 4 selected density-surface models (Table 1) binations of a maximum of 5 parameters, given 6 differed from the other candidate models chiefly in possible covariates), (2) common terns (‘CT’) over all habitat covariate influences (SST versus chlorophyll 3 surveys (126 combinations of 6 parameters given 7 or depth); only in the case of roseate terns did prey optional covariates; no roseate terns were identified covariates have a distinct effect on model selection in the fall 2010 survey), (3) common terns in the 2 (the only difference between the best and second- spring surveys (56 combinations of 4 parameters, best model was the influence of herring). Model 10 given 6 covariates), (4) roseate terns (‘RT’) in the 2 had an AIC value that did not differ significantly spring surveys (56 combinations). Additionally, mod- from its nested model (Table 1); given that model 10 els varied by distribution (Poisson or negative bino- was more complex (with the addition of 1 prey mial), and distance sampling engine (CDS or parameter, herring, to accompany sandlance), the MCDS). I used a backwards stepwise approach, likelihood ratio test evaluated it as significantly bet- starting with the ‘beyond optimal’ models (most ter (Johnson & Omland 2004). The combination of a complex, e.g. 7 co variates, 6 parameters), then sub- negative binomial distribution with MCDS produced sequently dropping 1 parameter. Once all covariates best-fit models only for roseate terns — although in the models reached significance (p < 0.05), I com- there were few 3- or 4-parameter candidate models pared nested models with likelihood ratio tests and that showed significance in all covariates, they had Goyert: Tern foraging: habitat, prey, and interspecies associations 295

Table 1. Density-surface model selection. The best models selected from the candidate set are shown in bold (with significant predictors shaded in gray) and indicate: the response variable; number of surveys analyzed; number of data cells sampled (n); distribution family (negative binomial: ‘Neg Bin’); type of distance sampling used in the detection (Detect.) function − either conventional (CDS) or multiple covariate distance sampling (MCDS); number of model parameters (Param.); significance of each covariate (***p < 0.001, **p < 0.01, *p < 0.05); the explained deviance (Dev.); and Akaike’s information criterion (AIC) value. Covariates for habitat (columns at left) are sea surface temperature (SST), chlorophyll concentration (Chl), and depth. Prey covariates (middle columns) are anchovy (An), herring (Hg), and sandlance (Sl). Other tern covariates (columns at right) are common tern Sterna hirundo and mixed terns (CMT) or roseate tern S. dougallii and mixed (RMT) terns. The ‘x’ indicates parameters that were not tested (i.e. not included in the data), ‘–’ indicates covariates that were not considered as predictors in the models shown (i.e. they were not significant in more complex models), spr: spring

Model Res- Sur- n Family Detect. Param. Habitat Prey Other tern Dev. AIC ponse veys SST Chl Depth An Hg Sl CMT RMT (%)

1 CRMT 3 55 Poisson CDS 5 *** – *** ** *** *** x x 94.2 360 2 52 Poisson CDS 4 – *** *** – *** *** x x 95.4 333 3 52 Poisson CDS 3 *** *** *** – – – x x 83.9 520 4 CT 3 52 Poisson CDS 5 *** *** – *** – *** x *** 96.5 297 5 52 Neg Bin CDS 5 – * *** – *** x * 48.3 373 6 52 Poisson CDS 4 – *** *** ––*** x *** 98.5 266 7 52 Neg Bin MCDS 4 – *** *** ––*** x *** 88.5 674 8 2 - spr 39 Poisson CDS 4 *** –– x* *** x *** 99.8 223 9 37 Poisson CDS 3 – *** *** x–*** x – 92.6 274 10 RT 2 - spr 40 Neg Bin MCDS 4 – – * x ** * *** x 95.3 209 11 40 Neg Bin MCDS 3 – – *** x–*** *** x 92.5 208 especially low AIC values; these unique properties numbers where intermediate SST, 8−10°C, charac- reflect the low incidence of roseate tern observations terized the habitat (Fig. 1). Of the selected 4 models, relative to common terns at sea. Overall, distance only in model 8 did SST emerge as a significant pre- sampling resulted in well-fit density-surface models dictor, stronger than depth or chlorophyll (note that I (high explained deviance, Table 1), and reasonable assigned depth a negative value, and it was posi- estimations of common tern abundance over the sur- tively correlated with SST and chlorophyll, such that vey area, yet it over-inflated roseate tern abundance shallow water embodied higher values). Addition- estimates, compared to the censused MA breeding ally, this model singly excluded bathy metry, suggest- population size (Table S1). ing that SST may sufficiently account for variation in Sandlance was the only covariate that influenced depth, given their co-dependence. Overall, higher all 4 selected models (Table 1, Fig. 1), demonstrating counts of common and roseate terns were likely to its strong effect on common and roseate tern distribu- occur where waters were shallow, less than 40 m tion and abundance. While model 10 suggests that deep, with variable sandlance abundance, and sam- roseate tern abundance had an inverse relationship pled herring numbers that reached 200 cell−1 (Fig. 1). with sandlance, model 2 suggests otherwise: com- The distribution of sandlance and herring (Fig. S1) mon, roseate, and mixed terns were likely to be ob - appeared to follow colder water than anchovies, as served at high and low values of sandlance (Fig. 1). supported by a negative correlation with SST (Fig. The grid cell between the island of Martha’s Vine- S3). Models 2 and 6 indicate that, across the 3 sur- yard and Buzzards Bay (Fig. S1b) gives an example veys, common terns, and apparently roseate terns, of where persistent sandlance abundance and ro - associated positively with chlorophyll concentration seate tern observations contributed to predictions of above 4 mg m−3 (with a peak at 6 mg m−3); since both relatively high roseate tern abundance in spring seasons were analyzed in these 2 models, this effect 2010 and 2011 (Fig. 2d). There were clear differences of primary productivity is attributable to the fall. between seasons, notably that no roseate terns were Unmistakably, the presence of neighboring con specific observed in the fall of 2010, which was characterized and heterospecific tern flocks shows co-dependency: by higher SST and more anchovies (Fig. S1); this sea- common terns aggregate with any number of roseate sonal increase in anchovy availability is supported by and mixed terns (RMT > 100, model 6; RMT < 100, the positive correlation between this prey category model 8); roseate terns assemble with intermediate and SST (Fig. S3). In the spring, common terns counts of common and mixed terns (CMT 50−300, (model 8, Table 1) were likely to be found in higher model 10). 296 Mar Ecol Prog Ser 506: 291–302, 2014

Fig. 1. Generalized additive model plots of the 4 selected models. The y-axes show the effects of the covariates (x-axes) on the response variables (fitted tern abundance), for all 3 surveys: (a) common tern Sterna hirundo, roseate tern S. dougallii, and mixed terns (CRMT; model 2), (b) common terns (CT; model 6); and the 2 spring surveys: (c) common terns (model 8), and (d) roseate terns (RT; model 10). Shaded areas demarcate the standard error bounds of uncertainty (confidence bands), and dotted lines delineate where y = 0. Habitat covariates are sea surface temperature (SST), chlorophyll concentration (Chl), and depth; prey covariates are anchovy (An), herring (Hg), and sandlance (Sl); other tern covariates are common and mixed terns (CMT) or roseate and mixed (RMT) terns

In the 2 spring surveys, common tern numbers DISCUSSION (mean ± SE: 19.1 ± 0.9; n = 1766) were observed over areas with significantly higher numbers of sampled This research demonstrates a clear relationship herring than roseate terns (8.7 ± 2.6; n = 97): t121.0 = among prey availability, habitat, and the social for- 3.7, p < 0.001 (n = 1863); however, comparisons be- aging behavior, distribution, and abundance of com- tween behavioral groups, within or between tern spe- mon and roseate terns. The distribution and abun- cies, were not significant for sampled herring numbers dance of principal prey items were associated (Fig. 3b). As for sandlance, the interaction be tween positively with the spatial patterns of common and tern species and behavior was significant (F1, 1863 = roseate terns, which supports the importance of her- 47.1, p < 0.001), where individual foraging roseate ring and sandlance to adults, and not just chicks (as terns were observed over areas with significantly established in colony-based provisioning studies, higher numbers of sampled sandlance (59.6 ± 10.0, Kirkham 1986, Safina et al. 1990, Tims et al. 2004, p < 0.001) than were foraging common terns (19.0 ± author’s unpubl. data). The relative spatial availabil- 1.2), and non-foraging common (22.1 ± 1.0) or roseate ity of sandlance was a key determinant of roseate terns (5.9 ± 1.9); individual foraging and non-foraging tern foraging behavior and ecology, in Massachusetts common terns were found over significantly more and, likely, the NW Atlantic Ocean. High abundance sandlance than non-foraging roseate terns (p < 0.01, of common terns predicted high abundance of Fig. 3a). All other behavioral group comparisons of roseate terns, and the reverse also occurred, suggest- sandlance and herring were insignificant (Fig. 3). ing that terns may be able to use each other as cues Goyert: Tern foraging: habitat, prey, and interspecies associations 297

Fig. 2. Predicted tern distribution and abundance in Massachusetts, USA, waters. The study region includes Cape Cod, the islands of Martha’s Vineyard (MV) and Nantucket (N), and Buzzards Bay, which contains the 3 largest shared breeding colonies of common tern Sterna hirundo and roseate tern S. dougallii on Bird, Ram, and Penikese Islands (d and dashed arrows); the ‘c’ on the ‘elbow’ of Cape Cod marks the location of a major common tern colony. Transect effort (black lines) is overlapped by counts of observed common, roseate, and mixed terns (circles). Thirty sampled grid cells (each 15 km × 15 km) were used in the density-surface modeling; white cells indicate missing covariate data (resulting in n = 28 for all 4 predictive grids). Fitted common, roseate, and/or mixed terns (log abundance per 225 km2 shaded grid cell) are based on predictions from the covariates corresponding to each of the 4 selected models, averaged across either all 3 surveys: (a) common, roseate, and mixed terns (CRMT; model 2), (b) common terns (CT; model 6); or the 2 spring surveys: (c) common terns (model 8), and (d) roseate terns (RT; model 10). The grid cell between MV and Buzzards Bay is outlined in (d) to give an example of where persistent sandlance abundance (see Fig. S1b in the Supplement) and roseate tern observations contributed to predictions of relatively high roseate tern abundance in spring 2010 and 2011 298 Mar Ecol Prog Ser 506: 291–302, 2014

roseate tern phenology, explaining, in part, the timing of chick-rearing and migration: why it might be important for chick-provisioning to occur while sandlance persist, and why roseate terns stage earlier than common terns (Nisbet et al. 2013). Nest provisioning studies have been widely used to assess chick diets (Barrett et al. 2007), and my study suggests that they can also reflect adult foraging in the weeks prior to peak hatch, since the spatial patterns of common and roseate terns in May overlapped with the distribution and abun- Fig. 3. Mean prey numbers by tern species and behavior across the 2 spring dance of those prey representative of inshore surveys. (a) Interaction between tern species and behavior was the dominant species later fed to chicks significant for sampled sandlance numbers (F1,1863 = 47.1, p < 0.001), where (in June and July 2010 and 2011, individual foraging roseate terns Sterna dougallii (RT) were observed over author’s unpubl. data), i.e. herring and areas with significantly higher numbers of sampled sandlance (59.6 ± 10.0, p < 0.001) than were foraging common terns S. hirundo (CT, 19.0 ± 1.2), and sandlance. With respect to the post- non-foraging common (22.1 ± 1.0) or roseate terns (5.9 ± 1.9), with mean breeding season, my speculation is that ± SE; individual foraging and non-foraging common terns were found over during their pre-migratory dispersal, significantly more sandlance than non-foraging roseate terns (p < 0.01); all when roseate terns have been observed other behavioral group comparisons of (a) sandlance and (b) herring were >100 km east of Cape Cod (Goyert et al. non-significant 2014), they pursue adult sandlance that move offshore (Robards et al. 2000), to the presence of prey, in line with the hypothesis which would explain the lack of roseate terns ob - that positive interspecies interactions may result served inshore during September. The association of from facilitation (e.g. local enhancement). Therefore, terns with shallow water likely related to improved the conservation and management of roseate terns prey accessibility, since terns have been known to depends not only on the availability of sandlance, but exploit tidal patterns across coastal shoals (Heine- also on the ecology of common terns. These findings mann 1992, Becker et al. 1993). Habitat strongly highlight the need to assess the health of forage fish affected common terns seasonally, where SST had a populations through proper management of commer- greater impact in the spring, and chlorophyll in the cial fisheries stocks (e.g. herring), or to designate fall. Primary productivity (chlorophyll) showed greater Marine Protected Areas (i.e. sandlance habitat) for importance in this study than in offshore surveys the protection of endangered species (roseate terns). (Goyert et al. 2014), likely due to an inshore coastal Sandlance distribution and abundance was the pri- effect, and the use of a larger scale to account for spa- mary predictor of the abundance and foraging be- tiotemporal lag in bottom-up trophic inter actions that havior of terns, among all covariates; flocks of other attract fish to plankton (e.g. a large scale allots more terns were secondary. The inconsistencies in the pos- room for trophic mismatch, as opposed to a fine scale, itive relationship between sandlance and common or Hunt & Schneider 1987, Grémillet et al. 2008). The roseate tern counts likely had more to do with unreli- behavioral relationship between foraging roseate ability in sandlance behavior and sampling regime terns and sandlance illustrates that terns may signal than in actual occurrence. The distribution and abun- the presence of prey, which supports the notion that dance of sandlance, caught at bottom depths, pro- terns rely on each other to find food. The aggregation vided a limited 2-dimensional index of availability of common and roseate terns with flocks of con- (Dänhardt & Becker 2011b) and, certainly, sandlance specifics and heterospecifics provides evidence for may have been accessible elsewhere in the water local enhancement: high-density mixed-species column (Dänhardt et al. 2011). The prevalence of flocks had a positive effect on the distribution and sandlance and herring in the spring (Fig. S1) fits their abundance of both roseate and common terns, sug- profile as colder-water species, as compared to gesting that facilitation may be at play, as opposed to anchovies (Garrison et al. 2002, Lucey & Nye 2010). I competition. Facilitation and competition can occur suspect that this places a temporal constraint on together, yet vary in intensity by scale and resource Goyert: Tern foraging: habitat, prey, and interspecies associations 299

availability (Fauchald et al. 2011): at coarse spatial primary productivity, resulting in habitat degrada- scales (as in this study), terns may attract each other tion or a northerly redistribution of prey, such as to feeding flocks (local enhancement; Erwin 1977, sandlance (Lucey & Nye 2010). A flexible foraging author’s unpubl. data), facilitating prey detection as response to such fluctuations would be required for long as prey remain abundant (Lack 1946, Langham common and roseate terns to search for food, given 1968, Dunn 1972, Poysa 1992, Buckley 1997, Ramos that they associate with SST and primary productiv- 2000); once those resources become limited, how- ity (models 2, 6, and 8). As opportunistic generalists, ever, then spatial partitioning may occur as a result of common terns are more likely than roseate terns to tern competition (Duffy 1986, Safina 1990). withstand drastic change over the long term (Mon- The advantage of using density-surface modeling tevecchi et al. 2009). However, model 10 suggests was its performance at predicting the distribution of that roseate terns may pursue prey in 3 ways: terns (Fig. 2); the disadvantage was its inflated abun- directly, via association with shallow water (indepen- dance predictions. The intrinsic nature of seabird dis- dently of SST and primary productivity), or by re - tributions likely explains why the GAM and distance maining in the vicinity of other mixed species terns sampling contribute to over-inflation in abundance flocks. If roseate terns opportunistically rely on social estimation. First, seabird aggregation patterns pro- facilitation like other seabirds (e.g. via local enhance- duce large counts at few covariate values, resulting in ment), then their chances of encountering prey are high fitted values, as predicted by the GAM (D. Miller improved (Grünbaum & Veit 2003). Alternatively, pers. comm.). Second, the problem may be inherent to rapid, unpredictable changes in sandlance distribu- using distance sampling with a biological population tion could result in prey limitation and allow tern such as seabirds (e.g. as opposed to whales, which competition to overpower the benefits and incidence presumably have a lower detection probability since of facilitative interactions (Safina & Burger 1988). they are below the surface). For example, a mean de- Redistribution of sandlance is a serious concern for tection probability of 25% (as in model 2), is low for an roseate terns, because these highly philopatric spe- experienced seabird observer scanning the 300−500 m cies would either expend too much energy traveling range, and 2% detection of roseate terns (model 10) is between the colony and distant foraging areas, caus- artificially low. MCDS seemed to over-compensate for ing chicks to starve, or they would have to endure attributing lack of visibility to sparse observations of nesting displacement, as they often have in the past roseate terns, by estimating high abundance from low (Gochfeld et al. 1998, Nisbet 2002). Prey depletion detection probability; low detection should have has compromised the breeding success of common matched more closely to low abundance. However, and roseate terns in the past (Safina et al. 1988) and MCDS did allow for exceptional fit in roseate terns has contributed to population declines (Szostek & (provided the appropriate distribution family), result- Becker 2012). Since the 1990s, herring stocks in the ing in a suitably complex model that retained biologi- NW Atlantic Ocean have generally followed a slowly cally meaningful variation instead of favoring parsi- increasing trend, in contrast to sandlance abun- mony-induced fit (Johnson & Omland 2004). Given its dance, which has been on the decline since the late strengths and weaknesses, DSM was an effective 1980s (Overholtz et al. 2000). Roseate terns were method of estimating seabird distribution and relative federally listed as endangered in 1987, and their pop- abundance, but users need to exercise caution in ulations currently show no improvement; therefore, making over-estimated predictions of absolute abun- further research should assess whether their pro - dance, especially with respect to the management of ductivity mirrors long-term historical trends in sand- roseate terns. lance, to address the extent to which prey sensitivity This study highlights the importance of sandlance may limit their potential for population recovery (Nis- to the distribution and abundance of roseate terns, bet & Spendelow 1999) — especially given that com- which raises concerns regarding the adaptability of mon terns have largely rebounded over the past few such a specialized endangered species, in response decades (Mostello 2012). It is important that we bet- to global climate change and fisheries pressure. On ter understand not only where common and roseate one hand, a potential top-down effect of global terns consistently forage across years, but how they warming, in the reduction of top marine predators, will respond to changes in prey availability. The could reduce consumptive impacts on pelagic forage miniaturization of enhanced tracking devices (Bur - fish, and perhaps increase their availability to terns ger & Shaffer 2008) should be able to provide a (Nye et al. 2013). A more likely outcome is the bot- means for future studies to better quantify tern uti- tom-up cascade of climatological shifts in SST and lization of foraging habitat; such information is 300 Mar Ecol Prog Ser 506: 291–302, 2014

essential to advancing the conservation and manage- Towards standardised seabirds at sea census techniques ment of these protected species. The sensitivity of in connection with environmental impact assessments for offshore wind farms in the U.K. Royal Netherlands Insti- spatial patterns in common, and especially roseate tute for Sea Research, Texel terns, to habitat, prey availability, and one another, Dänhardt A, Becker P (2011a) Herring and sprat abundance classifies them as conspicuous indicators of ecosys- indices predict chick growth and reproductive perform- tem, fisheries, and community processes (Einoder ance of common terns breeding in the Wadden Sea. Eco- systems 14: 791−803 2009). Quantifying the spatial relationships among Dänhardt A, Becker PH (2011b) Does small-scale vertical seabirds and their prey, in an ecosystem context, is distribution of juvenile schooling fish affect prey avail- essential to predicting long-term shifts in the distri- ability to surface-feeding seabirds in the Wadden Sea? bution and abundance of marine communities, for J Sea Res 65: 247−255 the purpose of marine spatial planning. Dänhardt A, Fresemann T, Becker P (2011) To eat or to feed? Prey utilization of common terns (Sterna hirundo) in the Wadden Sea. J Ornithol 152:347−357 Davoren GK, Montevecchi WA, Anderson JT (2003) Search Acknowledgements. I thank Jeremy King, Vinnie Manfredi, strategies of a pursuit-diving marine bird and the persist- and Matt Camisa at the Massachusetts Division of Marine ence of prey patches. Ecol Monogr 73: 463−481 Fisheries, who granted the opportunity to participate as a Diamond AW, Devlin CM (2003) Seabirds as indicators of volunteer seabird observer aboard the inshore bottom trawl changes in marine ecosystems: ecological monitoring on surveys, and also provided requested data. Carl Rhodes and Machias Seal Island. Environ Monit Assess 88: 153−175 the crew of the RV ‘Gloria Michelle’ accommodated me PubMed aboard their vessel. I am grateful to Dave Miller for offering Duffy DC (1986) Foraging at patches: interactions between technical assistance with density-surface modeling, and Kris common and roseate terns. Ornis Scand 17:47−52 Winiarski for supplying useful distance sampling resources. Dunn EK (1972) Studies on terns with particular reference to I appreciate guidance from Richard Veit and Lisa Manne feeding ecology. PhD dissertation, University of Durham with respect to analytical design, as well as comments from Einoder LD (2009) A review of the use of seabirds as indica- Carolyn Mostello, Jenny Basil, Mark Hauber, Jennifer Arnold, tors in fisheries and ecosystem management. Fish Res 95: and Bill Montevecchi. 6−13 Elliott KH, Bull RD, Gaston AJ, Davoren GK (2009) Under- water and above-water search patterns of an Arctic sea- LITERATURE CITED bird: reduced searching at small spatiotemporal scales. Behav Ecol Sociobiol 63:1773−1785 Amaral M, Saliva JE (2010) Caribbean roseate tern and Erwin RM (1977) Foraging and breeding adaptations to dif- North Atlantic roseate tern (Sterna dougallii dougallii): ferent food regimes in three seabirds: the common tern, 5-year review: Summary and evaluation. U.S. Fish and Sterna hirundo, royal tern, Sterna maxima, and black Wildlife Service, Concord, NH skimmer, Rynchops niger. Ecology 58: 389−397 Amorim P, Figueiredo M, Machete M, Morato T, Martins A, Fauchald P, Skov H, Skern-Mauritzen M, Hausner VH, Serrão Santos R (2009) Spatial variability of seabird dis- Johns D, Tveraa T (2011) Scale-dependent response tribution associated with environmental factors: a case diversity of seabirds to prey in the North Sea. Ecology 92: study of marine important bird areas in the Azores. ICES 228−239 J Mar Sci 66:29−40 Frederiksen M, Edwards M, Richardson AJ, Halliday NC, Barrett RT, Camphuysen K, Anker-Nilssen T, Chardine JW Wanless S (2006) From plankton to top predators: bot- and others (2007) Diet studies of seabirds: a review and tom-up control of a marine food web across four trophic recommendations. ICES J Mar Sci 64:1675−1691 levels. J Anim Ecol 75:1259−1268 Becker PH, Frank D, Sudmann SR (1993) Temporal and spa- Furness RW, Camphuysen K (1997) Seabirds as monitors of tial pattern of common tern (Sterna hirundo) foraging in the marine environment. ICES J Mar Sci 54: 726−737 the Wadden Sea. Oecologia 93: 389−393 Furness RW, Tasker ML (2000) Seabird-fishery interactions: Bjornstad ON (2009) ncf: Spatial nonparametric covariance quantifying the sensitivity of seabirds to reductions in functions. R package version 1.1-3. http://CRAN. R-project. sandeel abundance, and identification of key areas for org/package=ncf sensitive seabirds in the North Sea. Mar Ecol Prog Ser Buckley NJ (1997) Spatial-concentration effects and the 202: 253−264 importance of local enhancement in the evolution of Garrison LP, Michaels W, Link JS, Fogarty MJ (2002) Spatial colonial breeding in seabirds. Am Nat 149: 1091−1112 distribution and overlap between ichthyoplankton and Burger AE, Shaffer SA (2008) Perspectives in ornithology pelagic fish and squids on the southern flank of Georges application of tracking and data-logging technology in Bank. Fish Oceanogr 11: 267−285 research and conservation of seabirds. Auk 125:253−264 Gjerdrum C, Fifield DA, Wilhelm SI (2012) Eastern Canada Camphuysen CJ, Garthe S (2004) Recording foraging sea- Seabirds at Sea (ECSAS) standardized protocol for birds at sea: standardised recording and coding of forag- pelagic seabird surveys from moving and stationary plat- ing behaviour and multi-species foraging associations. forms. Canadian Wildlife Service, Atlantic Region, Dart- Atl Seabirds 6:1−32 mouth, NS Camphuysen CJ, Webb A (1999) Multi-species feeding Gochfeld M, Burger J, Nisbet ICT (1998) Roseate tern associations in North Sea seabirds: jointly exploiting a (Sterna dougallii). In: Poole A (ed) The birds of North patchy environment. Ardea 87: 177−198 America. Cornell Lab of Ornithology, Ithaca, NY. http:// Camphuysen CJ, Fox AD, Leopold MF, Petersen IK (2004) bna.birds.cornell.edu/bna/species/370 Goyert: Tern foraging: habitat, prey, and interspecies associations 301

Goyert HF, Manne LL, Veit RR (2014) Facilitative interac- indices on breeding performance of tropical roseate tions among the pelagic community of temperate migra- terns in the western Indian Ocean. Mar Ecol Prog Ser tory terns, tunas and dolphins. Oikos. doi: 10.1111/ oik. 351:273−286 00814 Mostello CS (2012) Inventory of terns, laughing gulls, and Grémillet D, Lewis S, Drapeau L, Van Der Lingen CD and black skimmers nesting in Massachusetts in 2011. MDFW, others (2008) Spatial match−mismatch in the Benguela NHESP, Westborough, MA upwelling zone: Should we expect chlorophyll and sea- Nisbet ICT (2002) Common tern (Sterna hirundo). In: Poole surface temperature to predict marine predator distribu- A (ed) The birds of North America. Cornell Lab of Or - tions? J Appl Ecol 45: 610−621 nithology, Ithaca, NY. http://bna.birds.cornell.edu/ bna/ Grünbaum D, Veit RR (2003) Black-browed albatrosses for- species/618 aging on Antarctic krill: density-dependence through Nisbet ICT, Spendelow JA (1999) Contribution of research local enhancement? Ecology 84: 3265−3275 to management and recovery of the roseate tern: review Heinemann D (1981) A range finder for pelagic bird census- of a twelve-year project. Waterbirds 22: 239−252 ing. J Wildl Manag 45: 489−493 Nisbet ICT, Veit RR, Auer SA, White TP (2013) Marine birds Heinemann D (1992) Foraging ecology of roseate terns of the eastern United States and the Bay of Fundy. Nut- breeding on Bird Island, Buzzards Bay, Massachusetts. tall Ornithological Monographs 29, Nuttall Ornithologi- USFWS, Manomet, MA cal Club, Cambridge, MA Hunt GL Jr, Schneider DC (1987) Scale-dependent pro- Nye JA, Gamble RJ, Link JS (2013) The relative impact of cesses in the physical and biological environment of mar- warming and removing top predators on the Northeast ine birds. In: Croxall JP (ed) Seabirds: feeding ecology US large marine biotic community. Ecol Model 264: and role in marine ecosystems. Cambridge University 157−168 Press, Cambridge, p 7–41 Overholtz WJ, Link JS (2007) Consumption impacts by mar- Jaquemet S, Le Corre M, Weimerskirch H (2004) Seabird ine mammals, fish, and seabirds on the Gulf of Maine− community structure in a coastal tropical environment: Georges Bank Atlantic herring (Clupea harengus) com- importance of natural factors and fish aggregating plex during the years 1977−2002. ICES J Mar Sci 64: devices (FADs). Mar Ecol Prog Ser 268: 281−292 83−96 Jaquemet S, Le Corre M, Quartly GD (2007) Ocean control Overholtz WJ, Link JS, Suslowicz LE (2000) Consumption of of the breeding regime of the sooty tern in the southwest important pelagic fish and squid by predatory fish in the Indian Ocean. Deep-Sea Res I 54:130−142 northeastern USA shelf ecosystem with some fishery Johnson JB, Omland KS (2004) Model selection in ecology comparisons. ICES J Mar Sci 57:1147−1159 and evolution. Trends Ecol Evol 19: 101−108 Poysa H (1992) Group foraging in patchy environments: the King JR, Camisa MJ, Manfredi VM (2010) Massachusetts importance of coarse-level local enhancement. Ornis Division of Marine Fisheries trawl survey effort, list of Scand 23: 159−166 species, and bottom temperature trends, 1978–2007. R Development Core Team (2012) R: a language and envi- MADMF, New Bedford, MA ronment for statistical computing, Version 2.15.0. R Kirkham IR (1986) Comparative foraging and breeding Foundation for Statistical Computing, Vienna. www.r- habits of Arctic and common terns. PhD dissertation, project.org Dalhousie University, Halifax, NS Ramos JA (2000) Characteristics of foraging habitats and Lack D (1946) Competition for food by birds of prey. J Anim chick food provisioning by tropical roseate terns. Condor Ecol 15: 123−129 102: 795−803 Langham NPE (1968) The comparative biology of terns, Robards MD, Willson MF, Armstrong RH, Piatt JF (2000) Sterna spp. PhD dissertation, University of Durham Sand lance: a review of biology and predator relations Le Corre M, Jaquemet S (2005) Assessment of the seabird and annotated bibliography. USDA Forest Service, community of the Mozambique Channel and its potential Pacific Northwest Research Station, Portland, OR use as an indicator of tuna abundance. Estuar Coast Roberts J, Best B, Dunn D, Treml E, Halpin P (2010) Marine Shelf Sci 63:421−428 geospatial ecology tools: an integrated framework for Lucey SM, Nye JA (2010) Shifting species assemblages in ecological geoprocessing with ArcGis, Python, R, MAT- the Northeast US Continental Shelf Large Marine LAB, and C++. Environ Model Softw 25: 1197−1207. Ecosystem. Mar Ecol Prog Ser 415: 23−33 http://mgel.env.duke.edu/mget Miller DL (2012) Distance: a simple way to fit detection func- Rock JC, Leonard ML, Boyne AW (2007) Foraging habitat tions to distance sampling data and calculate abun- and chick diets of roseate tern, Sterna dougallii, breed- dance/density for biological populations, Version 0.7.1. ing on Country Island, Nova Scotia. Avian Conserv Ecol http://CRAN.R-project.org/package=Distance 2: 4. www.ace-eco.org/vol2/iss1/art4/ Miller DL, Burt ML, Rexstad EA, Thomas L (2013a) Spatial Safina C (1990) Bluefish mediation of foraging competition models for distance sampling data: recent developments be tween roseate and common terns. Ecology 71: and future directions. Methods Ecol Evol 4: 1001−1010 1804−1809 Miller DL, Rexstad E, Burt L, Bravington MV, Hedley S (2013b) Safina C, Burger J (1988) Ecological dynamics among prey dsm: Density surface modelling of distance sampling fish, bluefish, and foraging common terns in an Atlantic data, Version 2.0.1. Available at http://github. com/dill/ coastal system. In: Burger J (ed) Seabirds and other Montevecchi WA, Benvenuti S, Garthe S, Davoren GK, Fifield marine vertebrates: competition, predation, and other D (2009) Flexible foraging tactics by a large opportunistic interactions. Columbia University Press, New York, NY, seabird preying on forage- and large pelagic fishes. Mar p 95–173 Ecol Prog Ser 385: 295−306 Safina C, Burger J, Gochfeld M, Wagner RH (1988) Evi- Monticelli D, Ramos JA, Quartly GD (2007) Effects of dence for prey limitation of common and roseate tern annual changes in primary productivity and ocean reproduction. Condor 90: 852−859 302 Mar Ecol Prog Ser 506: 291–302, 2014

Safina C, Wagner RH, Witting DA, Smith KJ (1990) Prey and newly-established colonies. Waterbirds 27: 321−332 delivered to roseate and common tern chicks; composi- Weimerskirch H (2007) Are seabirds foraging for unpre- tion and temporal variability. J Field Ornithol 61: 331−338 dictable resources? Deep-Sea Res II 54: 211−223 Shealer DA, Kress SW (1994) Postbreeding movements and Weimerskirch H, Bertrand S, Silva J, Marques JC, Goya E prey selection of roseate terns at Stratton Island, Maine. (2010) Use of social information in seabirds: Compass J Field Ornithol 65: 349−362 rafts indicate the heading of food patches. PLoS ONE 5: Szostek K, Becker P (2012) Terns in trouble: demographic e9928 consequences of low breeding success and recruitment Williams CT, Whittam B, Purvis M (2009) The nearshore dis- on a common tern population in the German Wadden tribution of terns and other seabirds in relation to indus- Sea. J Ornithol 153:313−326 trial project development in Stormont Bay, Nova Scotia. Tasker ML, Hope-Jones P, Dixon T, Blake BF (1984) Count- Bird Studies Canada, Atlantic Region, Sackville, NB ing seabirds at sea from ships: a review of methods and a Wood SN (2006) Generalized additive models: an introduc- suggestion for a standardized approach. Auk 101: 567−577 tion with R. Chapman & Hall/CRC, New York, NY Thomas L, Buckland ST, Rexstad EA, Laake JL and others Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data ex- (2010) Distance software: design and analysis of distance ploration to avoid common statistical problems. Methods sampling surveys for estimating population size. J Appl Ecol Evol 1:3−14 Ecol 47: 5−14 Zuur AF, Saveliev AA, Ieno EN (2012) Zero inflated models Tims J, Nisbet ICT, Friar MS, Mostello C, Hatch JJ (2004) and generalized linear mixed models with R. Highland Characteristics and performance of common terns in old Statistics, Newburgh

Editorial responsibility: Yves Cherel, Submitted: November 5, 2013; Accepted: April 24, 2014 Villiers-en-Bois, France Proofs received from author(s): June 12, 2014