Support for the Trophic Theory of Island Biogeography Across Submarine Banks in a Predator-Depleted Large Marine Ecosystem

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Vol. 607: 155–169, 2018 MARINE ECOLOGY PROGRESS SERIES Published December 6 https://doi.org/10.3354/meps12799 Mar Ecol Prog Ser

OPENPEN ACCESSCCESS Support for the trophic theory of island biogeography across submarine banks in a predator-depleted large marine ecosystem

C. H. Stortini1,*, K. T. Frank1,2, W. C. Leggett1, N. L. Shackell2, D. G. Boyce3

1Department of Biology, Biosciences Complex, Queen’s University, 116 Barrie St., Kingston, ON K7L 3N6, Canada 2Fisheries and Oceans Canada, Bedford Institute of Oceanography, 1 Challenger Dr., Dartmouth, NS B2Y 4A2, Canada 3Ocean Frontier Institute, Steele Ocean Sciences Building, Dalhousie University, 1355 Oxford St., PO Box 15000, Halifax, NS B3H 4R2, Canada

ABSTRACT: The trophic theory of island biogeography (TTIB) predicts that when predators are depleted, prey extinction rates decrease, leading to increases in prey alpha diversity and an increase in the slope of the species−area relationship (SAR). The TTIB has been tested and supported in a restricted set of systems at small spatial scales (0.25 m3 [reef patches] to 29 500 m2 [terrestrial]). Across semi-insular fish communities on 10 offshore banks ranging in size from 534 to 10 537 km2 on the Scotian Shelf (northwest Atlantic Ocean), we found support for the predictions of the TTIB. The prey SAR slope was significantly higher after the collapse of large predator populations than before the collapse, due largely to the immigration (or colonization) of many new prey species, principally on the largest banks. Coincident increases in core (resident) prey species densities, primarily on the largest banks, suggests that extinction risk decreased. The appearance of a strong SAR within the mesopredator trophic group in the post-predator collapse era (r2 = 0.55 relative to 0.12 in the pre-collapse era) suggests that the TTIB may also apply to mesopredator release in insular marine communities. Increases in mesopredator densities coincident with the colonization of previously unoccupied banks by core mesopredator species suggests that range expansions contributed to the increased strength of the SAR. Our study contributes to our evolving understanding of island biogeography theory and suggests that TTIB may provide a useful framework for evaluating trophic alterations in large marine (and non-marine) ecosystems.

KEY WORDS: Alpha diversity · Marine · Fish · Predator−prey · Species−area relationship · Diversity · Trophic theory · Island biogeography · Mesopredator release

INTRODUCTION gration rate increases with island area and decreases with isolation, while extinction rate decreases with The increase in alpha diversity (the number of spe- island area and increases with isolation. It is becom- cies) with habitat area is considered one of the foun- ing increasingly recognized that these rates, and dations of theoretical ecology (MacArthur & Wilson subsequently the parameters of the SAR, vary with 1967, Connor & McCoy 1979). The classic equilib- species interactions, such as predator−prey interac- rium theory of island biogeography (ETIB) attributed tions, and species traits (body size, diet generality, this ‘species−area relationship’ (SAR) to the scaling and trophic group; Drakare et al. 2006, Ryberg & of species immigration and extinction rates with Chase 2007, Holt 2009, Ryberg et al. 2012, Jacquet et habitat area and isolation (MacArthur & Wilson al. 2017). The trophic theory of island biogeography 1967). Assuming that all species are equal, the immi- (TTIB; Ryberg & Chase 2007, Holt 2009, Ryberg et al.

© The authors 2018. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 156 Mar Ecol Prog Ser 607: 155–169, 2018

Fig. 1. Predictions of the trophic theory of island biogeography adapted to marine fish communities. (a) Assuming a constant immigration rate (blue line), the presence of large-bodied predators increases extinction rates (red lines) within prey communities, thereby reducing alpha diversity (number of different coloured fishes, and the point at which immigration and extinction rates intersect, as indicated by black, vertical dashed lines) of small-bodied prey on both small and large 'islands'; the small number of prey species overall leads to a smaller difference in alpha diversity between small (αsmall) and large (αlarge) islands (a smaller species–area relationship [SAR] slope). (b) When large-bodied predators are absent, prey extinction rates decline and alpha diversity increases, especially on large 'islands', leading to a greater difference in alpha diversity between small (αsmall) and large (αlargel) islands, and therefore, an increase in SAR slope

2012) predicts that when large-bodied predators are Macro-ecological studies conducted on the Scotian depleted, the slope of prey community SARs should Shelf/Gulf of Maine region of the Northwest Atlantic increase due to reductions in prey extinction rates Ocean, at scales ranging from 172 000−300 000 km2, (Fig. 1; Ryberg & Chase 2007, Ryberg et al. 2012, have yielded initial insights into the response of fish Chase et al. 2009). communities to fishing-related perturbations. Here, a Since the publication of Ryberg & Chase’s (2007) precipitous and prolonged collapse of large-bodied TTIB, there have been only a small number of empir- predatory fish populations occurred in the early ical tests of the theory, which have spanned a limited 1990s as a consequence of overfishing (Choi et al. range of ecosystem types, and which occurred at 2005, Frank et al. 2005, 2011). Shackell et al. (2012) small spatial scales. Ryberg & Chase (2007) found reported that similarity among neighboring commu- that the absence of lizard and fish predators resulted nities of 20 common large-bodied fish species pro- in a significant increase in the slope of SARs of insect gressively declined, concomitant with a reduction in and zooplankton prey species in terrestrial glades average body size due to size-selective fishing. Sub- ranging in size from 750−29 500 m2 and in freshwater sequently, Ellingsen et al. (2015) found that as the ponds ranging in size from 92−5834 m2. Stier et al. regional occupancy of a dominant predator (Atlantic (2014) reported that reef patches (ranging from 0.25 cod Gadus morhua) declined, both alpha and beta to 0.5 m3) on which predatory groupers (Cephalopho- diversity of all remaining fish species increased. lis argus) were experimentally removed exhibited However, neither study evaluated the potential that significantly higher alpha and beta diversities of the trophic interactions or changes in the spatial scaling remaining fish species compared to reef patches of diversity within trophic groups contributed to the with groupers. However, at this scale and small community responses to the collapse of large-bodied range of patch sizes, reef patch area did not influence predators. Moreover, in both cases, the regional fish the response. More recently, Johnston et al. (2016) community composition was characterized by a mix- reported that the presence of ciliate predators (Eu - ture of species occupying different habitats, and in plotes aediculatus and Stentor coeruleus) reduced the study by Shackell et al. (2012), the species con- prey (1 flagellate and 6 ciliate species) alpha diver- sidered represented only a small subset of the total sity in a mesocosm meta-community of protists. species pool (<20%). Stortini et al.: Island biogeography in large marine ecosystems 157

Here, we build upon these findings by testing the of habitat area in shaping marine fish community predictions of TTIB across 10 semi-insular (Frank & responses to predator depletion and place a stepping Shackell 2001), highly productive, offshore banks on stone on the path toward a broader understanding the Scotian Shelf in the northwest Atlantic Ocean. of the processes underlying these community-level These banks were dominated by predatory ground- responses. fish species prior to their collapse in the early 1990s, which triggered an ecological regime shift (Frank et al. 2005, 2011). We tested the prediction that the MATERIALS AND METHODS slope of prey species SAR increased following the collapse of large-bodied predator populations on the Offshore banks banks. We also tested the hypothesis that the slope of mesopredator species SAR increased, as this group The offshore banks of the northwest Atlantic Ocean may have experienced a release from competition have been recognized as important and productive following large-bodied predator collapse (‘meso pre - fishing grounds for centuries. In contrast, their ecolog- dator release’; e.g. Crooks & Soulé 1999). Finally, we ical significance as ‘underwater islands’ has garnered assessed temporal changes in bank community struc- less attention (but see Frank & Shackell 2001). The ture and trophic group-specific densities to evaluate offshore banks of the Scotian Shelf (<100 m depth, the extent to which changes in alpha diversity were ranging in area from 534−10 537 km2; Fig. 2) constitute driven by expansion of core species and/or immigra- the preferred summer habitat and principal nursery tion of new species following the predator collapse. areas of many formerly dominant, and highly ex- Given the global nature of marine predator deple- ploited, large-bodied predator species (Shackell & tion (Worm et al. 2009, Juan-Jordá et al. 2011), body Frank 2000, Ricard & Shackell 2013). The maximum size reductions and consequent diminishing of pre- and average separation distance between these dation efficiencies (Scharf et al. 2000, Shackell et al. banks is 640 and 280 km, respectively. Their average 2010), species introductions (Bax et al. 2003, Cheung depth ranges from 60 to 90 m, while the depth of sur- et al. 2009), and the likelihood of variation in commu- rounding waters averages 142 m. Recirculation fea- nity responses among ecosystems (e.g. keystone pre- tures (Loder et al. 1988, Cong et al. 1996) act to retain dation; Paine 1966), it is important that the predic- larval fish on these banks and thus contribute to popu- tions of TTIB continue to be tested at various scales lation structuring at this scale (Frank 1992). This re- and in a variety of ecosystem types. A greater under- sults in a high level of community insularity. standing of how, why, and when classic ecological The dissimilarity between bank fish communities theories do, or do not, apply to various ecosystems and adjacent deeper-water communities indicates will permit a broader understanding of the conse- that these banks function as discrete habitat ‘islands’ quences of human disturbance. In turn, this will lead to improved management and restoration practices (e.g. Palmer et al. 1997). It is widely understood that large predators are a necessary component of ecosystems, facilitating balance and stability, and keeping lower trophic levels in check. The development of the ‘large fish indicator’ as an indicator of ecosystem health (Shephard et al. 2011, Mod- ica et al. 2014) is a testament to the global evolution of thought in this direc- tion. However, current understanding of the biogeography of community re - sponses to predator depletion, particularly at lower trophic levels, remains limited. By testing TTIB in a large mar- Fig. 2. Offshore banks of the Scotian Shelf. Topographical (depth) data were obtained from the Canadian Hydrological Service. Bank boundaries are de- ine ecosystem across semi-insular com- fined by the 100 m isobath and have been routinely sampled by the Fisheries munities, we sought to uncover the role and Oceans Canada summer trawl survey (Fig. S2 in Supplement 1) 158 Mar Ecol Prog Ser 607: 155–169, 2018

bounded in ecological space (Supplement 1 at www. survey strata (Fig. S2). Several secondary charac- int-res.com/articles/suppl/m607p155_supp.pdf for all teristics (Supplement 2) of the banks were evalu- supplements). This concept is supported by the work ated as potential determinants of alpha diversity of Frank & Shackell (2001), who documented the (see Supplement 6). existence of a strong (r2 = 0.81) SAR across the Scot- ian Shelf bank fish communities. In addition, they reported a strong positive correlation (r2 = 0.58) Trophic groups between alpha diversity and population densities. Consistent with the predictions of ETIB (MacArthur In marine fishes, body size is generally propor- & Wilson 1967), this implied that the larger banks tional to trophic level (Romanuk et al. 2011). In north- had lower extinction rates relative to smaller banks. west Atlantic temperate marine ecosystems, most Consequently, these banks would appear to be the dominant predatory groundfish species consume a ideal case study for testing the TTIB in a large marine wide range of prey items throughout the year, de - ecosystem. pending on availability and predator gape size (Link & Almeida 2000). Due to gape size constraints, individual predators tend to eat prey items less than or Description of the data equal to 50% of their body size (Scharf et al. 2000, Costa 2009). Given that each of the large-bodied Records of species identity, presence/absence, predators had an average recorded maximum length abundance, and individual body lengths for the fish per tow of >60 cm, their prey were conservatively communities of each of the 10 offshore banks of the defined as all species with an average maximum Scotian Shelf ecosystem (Fig. 2) were derived from length per tow of <31 cm. By extension, species with scientific trawl surveys that span most of the benthic an average maximum length per tow between 31 and Scotian Shelf ecosystem and have been conducted 60 cm were defined as mesopredators. In only 1 case annually during July since 1970 (DFO 2016). While (Atlantic mackerel Scomber scombrus), body size did some areas of the Shelf with very rugged topography not reflect trophic level; this species was included in and steep slopes have been less consistently sam- the prey trophic group (Supplement 3). Commercial pled, the banks, which are characterized by rela- mesopredators (haddock Melanogrammus aeglefi- tively uniform depths, have been consistently and nus, redfish [Sebastes spp.], American plaice Hip- effectively sampled. Trawls were deployed at ran- poglossoides platessoides, and cusk Brosme brosme; dom locations within pre-determined sampling areas shown as commercial [‘C’] in Table S1) were re - (strata) stratified by depth (Fig. S2 in Supplement 1). moved from the analyses in order to limit bias related Standardized sampling methods ensured that annual to the ongoing exploitation of these species. In effect, effort was generally proportional to stratum area (for these mesopredators are predated upon by humans, details see Doubleday & Rivard 1981). In our alpha and so their response to large predator depletion diversity estimations, only individuals identified to would likely be dampened. From this point onward, the species level were included (except for redfish, the mesopredator trophic group refers only to non- which constitutes 2 species that are not easily distin- commercial mesopredators, i.e. those species that are guished, i.e. Sebastes mentella and S. fasciatus). Due not consistently commercially fished on the banks. to variation in the distance trawled per sample, we multiplied each abundance and biomass record by the ratio of standard tow distance (1.75 km) to the Pre- and post-collapse regime definition actual distance towed. This standardized all abundance and biomass records to the standard sample At the scale of the entire Scotian shelf, Bundy et area (0.04 km2), thereby limiting sampling bias in our al. (2009) and Frank et al. (2011) reported an eco- temporal analyses. logical regime shift, characterized by significant The habitat of each bank was characterized using increases in the biomass of forage fish species and data collected during Fisheries and Oceans Canada macroinvertebrates, in the early 1990s following (DFO) scientific trawl surveys and by the Canadian the collapse of previously dominant predator spe- Hydrographic Service. The primary variable of cies. Body sizes, condition, and population growth interest, the area of each bank, was quantified rates of large-bodied predatory fish declined using ArcMap 10.5 (ESRI), given the boundaries across both western and eastern halves of the shelf defined by depth in the design of DFO’s July trawl and have yet to re cover to their pre-collapse states Stortini et al.: Island biogeography in large marine ecosystems 159

(Shackell & Frank 2007, Shackell et al. 2010), al- cies only observed in 1 of n tows. Total alpha diver- though some recovery of smaller-bodied, commer- sity per bank, per regime, was calculated as the cially exploited mesopre dators has been evident cumulative Se, when n = N (total number of tows). (Frank et al. 2011). We confirmed that the tem - The sampling variance associated with estimates of poral changes in the annual densities (average alpha diversity were calculated, according to Smith & abundance per survey tow) of large-bodied preda- van Belle (1984), as: tors, mesopredators, and prey at the scale of the N f N −1 banks were consistent with these shelf-wide dy - var = a2 − 1 (2) Se ∑ n=1 1 N N namics (see Fig. 3). We were therefore able to () explicitly define predator-dominant and predator- where a1 is the number of species observed only once depleted time periods (i.e. pre- and post-collapse in n number of tows, and f1 is the total number of regimes) for our analyses. These analyses (com- species observed only once across all N tows. pleted using R version 3.4.3; R Core Team 2017) The bank-specific Jackknife 1 alpha diversity esti- also quantified the population dynamics of prey mates constituted the dependent variable for our de - and mesopredator populations in the pre- and rived SARs. A semi-log model (Gleason 1922) yielded post-collapse regimes. the best fit to our data (largest r2) compared to alternative SAR model formulations, including Arrhenius, Lomolino, and Gitay (see Dengler 2009 for an over - Slope of the SAR view). The regime-specific SARs took the following form: We tested the prediction, based on TTIB, that the S = k + z(log (A)) (3) collapse of large-bodied predators across the banks e 10 would induce a higher SAR slope for both prey and where Se is the Jackknife-estimated cumulative alpha mesopredator trophic groups in the post-collapse diversity per bank, k is the estimated intercept, z is regime relative to the pre-collapse regime. Due to the the slope, and A is bank area measured in km2. A limited sampling effort on some smaller banks (e.g. multivariate model with a bank area-regime inter - 2 tows yr−1 on Baccaro and Roseway Banks), an analy- action term was used to test for a significant change sis of annual SARs was not feasible. Alpha diversities in SAR slope between regimes (ANCOVA). In both of prey and mesopredator species were estimated for uni variate and multivariate models, each Se was each bank in each regime (1970−1991 and 1992− weighted by the inverse of its corresponding vari-

2016) using the Jackknife 1 estimator in the ‘vegan’ ance (1/varSe), such that alpha diversity estimates package in R version 3.4.3 (‘specpool();’ Oksanen et with larger error were weighted less heavily in the al. 2017, R Core Team 2017). Several other alpha di- models. Both univariate and multivariate linear mod- versity estimators were compared (Supplement 4). els were generated using the base package in R ver- The relative alpha diversities of the banks in both pre- sion 3.4.3 (R Core Team 2017). 1992 and post-1991 regimes were consistent across The potential ability of other bank habitat charac- estimators; the Jackknife 1 estimate was middle range teristics (Supplement 2) to explain residual variabil- and offered low associated error (Supplement 4). The ity in alpha diversity was tested for using Akaike’s Jackknife 1 estimator (Smith & van Belle 1984) accu- information criterion corrected for small sample sizes mulates species richness across randomly selected (AICc; Mazerolle 2016) step-wise model selection, tows and then adds an estimated number of species after accounting for collinearity among predictors that were likely undetected. The estimated number of using a sequential regression approach (Graham (n–1) undetected species (a1––––n ) is based on the number of 2003, Dormann et al. 2013, Boyce et al. 2015; see species that were sampled only once during the se- Supplement 6). Sequential regression involves the lected period (a1, Eq. 1 below). Alpha diversity was es- regression of highly collinear predictor variables timated as the cumulative number of species (plus (e.g. predictor 1 and predictor 2), and the inclusion of those undetected), as follows: residuals from this regression as a predictor in the model of alpha diversity, representing the residual (n− 1) SSeo=+ a 1 (1) effect of predictor 2 without double-counting the {}n aspects of this variable that are collinear with the where Se is the estimated alpha diversity per cumula- other, fully represented predictor 1. Models were tive number of survey tows (n), So is the number of generated and assessed using R version 3.4.3 (R Core species observed per n, and a1 is the number of spe- Team 2017). 160 Mar Ecol Prog Ser 607: 155–169, 2018

Towards a mechanistic understanding of changes appearances of species from the banks in the post- in SAR slope 1991 era were also examined and contrasted to the appearances of new species. Central to the TTIB is the hypothesis that increases in the slope of prey SARs result from reduced extinction rates when predators are absent or depleted RESULTS (Fig. 1). To gain insight into the potential mechanisms driving observed changes in prey and mesopredator Pre- and post-collapse regime definition SARs across the Scotian Shelf banks, we evaluated whether changes in alpha diversity were accompanied Our analyses revealed that annual abundance by changes in density (abundance per unit area). Ex- (standardized per tow) anomalies for the large-bod- tinction risk decreases as population sizes increase ied predator trophic group were generally positive (Frank & Brickman 2000, Dulvy et al. 2004, Hutchings on all of the banks until the early 1990s. During & Reynolds 2004), and larger habitats provide more this interval, 25% of the annual anomalies were, on area and a greater amount of resources to allow for average, >1 standard deviation (SD). Following this population growth and maintenance (MacArthur & period, the predator abundance anomalies were gen- Wilson 1967). Frank & Shackell (2001) noted that the erally negative with 26%, on average, >1 SD (Fig. 3). larger banks supported higher densities of fish in gen- Conversely, small-bodied prey species exhibited general, compared to smaller banks, implying that larger erally negative anomalies across all of the banks until banks not only provided more area for population the early 1990s and positive thereafter, with the fre- growth but also more resources per unit area. There- quency of annual anomalies >1 SD averaging 28% fore, if the slope of the prey (and/or mesopredator) (Fig. 3). Negative prey anomalies were infrequent species SAR increased in the wake of predator col- during the post-predator collapse regime, and, when lapse, we would expect that prey (and/or mesopreda- they occurred, were always <1 SD. In both cases tor) density would also increase, particularly on large (predator and prey), the transition between negative banks. For both prey and mesopredator groups, aver- and positive standardized anomalies oc curred around age abundance per tow was calculated per year (and 1991 (±3 yr) across all 10 banks (Fig. 3). We con- per regime) on each bank and was evaluated in rela- cluded that it is reasonable to consider the 1970−1991 tion to the raw species counts per year (and alpha di- pe riod as a predator-dominated state (hereafter, ‘pre- versity estimates per regime). 1992’) and the 1992−2016 period a predator-depleted Although the classic TTIB assumes a constant im - state (hereafter, ‘post-1991’) across the banks. migration rate, we explored the potential for in - Shifts in non-commercial mesopredator abundance creased immigration or successful colonization of were not as dramatic, but a small increase in abun- prey and mesopredator species during the post-1991 dance was evident across the majority of the banks in regime. Trophic group compositions (including the the post-1991 era, particularly on Brown’s and West- frequency of tows in which each species was ob- ern Banks (Fig. 3). On average, a small proportion of served) were examined on each bank during each mesopredator abundance anomalies (15%) were >1 regime. Post-1991 appearances of species within SD in the post-collapse regime; an even smaller pro- prey and mesopredator groups that were not ob - portion of anomalies were <−1 SD (9%). This differed served on individual banks in the pre-1992 regime from the more even dispersion of anomalies in the were noted. Their pre-1992 frequency of observation pre-1992 era (on average, 10% were >1 SD, and 12% on other banks, or off-bank areas, were also consid- were <−1 SD). ered. These occurrences suggested potential migration or range expansion (suggesting reduced local extinction risk) of some species from other banks, Slope of the SAR and potential immigration or successful colonization of others from off-bank areas or other regions. Our Prey species SARs were significant in both the pre- assessment of changes in the correlation of bank 1992 (r2 = 0.51 p < 0.05) and the post-1991 regime community dissimilarities (using Bray-Curtis dissimi- (r2 = 0.83, p < 0.001), but were much stronger in the larity; ‘vegan’ package in R version 3.4.3; Oksanen post-1991 regime (Table 1). Consistent with TTIB, et al. 2017, R Core Team 2017), with geographic the slope of the prey species SAR was significantly distance between bank centroids, provided further (p < 0.05) higher in the post-1991 era (Fig. 4a; refer to insight into the origin of newly observed species. Dis- the significance of the area:regime interaction term Stortini et al.: Island biogeography in large marine ecosystems 161

Fig. 3. Standardized annual density (abundance tow−1) anomalies (measured in standard deviations from the long-term mean, SD units) for large-bodied predators, prey, and mesopredators (trophic groups) on each of the 10 offshore banks arranged from the smallest (top) to largest (bottom): Baccaro (Bc), Roseway (Rw), La Have (LH), Emerald (Em), Brown’s (Bw), Middle (Md), Western (Ws), Misaine (Mi), Banquereau (Bq), and Sable (Sb). Values were standardized and the anomaly was calculated ac- s cording to V i = (Vi − VAve)/VSD, where Vi represents the density in year i, the superscript s represents the standardized anomaly, VAve is the trophic group’s long-term (1970−2016) average density on the bank, and VSD is the associated standard deviation (SD). Grey horizontal lines mark ±1 SD. The blue vertical dotted line in each column marks the year 1991, separating pre-1992 and post-1991 regimes in the ANCOVA model in Table 1). This was due to variability in among-bank estimates of prey alpha an approximate doubling of prey alpha diversity on 6 diversity (Supplement 6). of the 10 banks: Brown’s (Bw), Misaine (Mi), Ban- The mesopredator SAR was not significant in the quereau (Bq), Middle (Md), Sable (Sb), and Western pre-collapse regime (r2 = 0.12, p = 0.33), but was sig- (Ws) banks, a response to large-bodied predator de - nificant in the post-collapse regime (r2 = 0.55, p < pletion (Frank et al. 2013). Through their interaction 0.05) (Table 1; Fig. 4b). This resulted largely from (in the multivariate model; ANCOVA), bank area increases in alpha diversity on the largest banks and regime explained a significant proportion of (+38% on Bq, +17% on Bw, +63% on Mi), decreases variance in prey alpha diversity (adjusted r2 = 0.80, on 1 of the smallest banks (−37% on Rw), and limited p < 0.001; Table 1). For both univariate (regime- changes in alpha diversity elsewhere. In the multi- specific) and multivariate (ANCOVA) models, as - variate model (ANCOVA), the interaction of bank sumptions of normality and homoscedasticity were area and regime explained 28% (adjusted r2) of the upheld, and no sign of non-linearity was evident variation in mesopredator alpha diversity (p < 0.05; (Supplement 5). No other bank habitat characteris- Table 1). This was due to a non-significant (p = 0.245; tics contributed meaningfully to the limited residual Table 1) increase in the slope of the mesopredator 162 Mar Ecol Prog Ser 607: 155–169, 2018

Table 1. Univariate, regime-specific species−area relationship (SAR) models SAR in the post-1991 regime, relative and multivariate ANCOVA models for both prey and mesopredator trophic to the pre-1992 regime (refer to the groups. Bank area was log10 transformed to obtain a linear fit; the semi-log interaction term in the ANCOVA model (Gleason 1922) performed best compared to all other alternative SAR models. In the ANCOVA models, the area:regime interaction term accounts model, Table 1), in which the slope for any changes in the effect of area on species accumulation (SAR slope) was not significantly different from 0 between regimes. The proportion of variance explained (r2) and p-values of (Fig. 4b; refer to pre-1992 estimate of each model are given, as are the parameter estimates and p-values for the area coefficient, i.e. SAR slope, and individual predictors. The parameter estimate for area in the SAR models rep- corresponding p-value, Table 1). As - resents the slope (z) of the relationship. The parameter estimate for the area:regime interaction term of the ANCOVA models represents the change sumptions of normality and homo - in slope between regimes. The p-value associated with this estimate indicates scedasticity were upheld (Supple- whether the change in SAR slope between regimes was significantly (p < 0.05) ment 5). No bank habitat characteris- different from 0 tic, other than bank area, contributed meaningfully to explaining variability 2 Trophic group/model r p Predictor Estimate p in the mesopredator alpha diversity (Supplement 6). Prey To evaluate the sensitivity of our Pre-1992 SAR 0.51 <0.05 Intercept −20.37 0.109 results to our definition of the 2 re - log10(area) 9.78 <0.05 Post-1991 SAR 0.83 <0.001 Intercept −47.10 <0.01 gimes, we constructed prey and meso - predator SARs within 20 and 15 yr log10(area) 21.92 <0.001 ANCOVA 0.80 <0.001 Intercept −45.84 <0.01 moving windows (Supplement 7). We

log10(area) 21.81 <0.001 were then able to evaluate temporal Regime 26.00 0.161 trends in SAR slope (z) (Supple- log10(area):regime 11.89 <0.05 ment 7). In general, we found that Mesopredator prey SARs from time periods con- Pre-1992 SAR 0.12 0.33 Intercept 4.97 0.500 strained to the pre-1992 regime had log10(area) 2.15 0.331 significantly lower slope values than Post-1991 SAR 0.55 <0.05 Intercept −4.88 0.410 SARs from time periods strictly within log10(area) 5.39 <0.05 the post-1991 regime. SAR slopes in ANCOVA 0.28 <0.05 Intercept −4.88 0.411 time periods spanning both pre- and log10(area) 5.40 <0.01 Regime 9.85 0.287 post-collapse regimes were interme - diate (Supplement 7). With shorter log10(area):regime 3.25 0.245 (15 yr) windows, the transition period

Fig. 4. Species−area relationships (SARs) for (a) prey and (b) mesopredators in the pre-collapse (grey) and post-collapse (red) regimes. Error bars represent 95% confidence intervals for each estimate of alpha diversity. The dashed lines surrounding the linear SAR trends (solid lines) represent the 95% confidence intervals associated with the regime-specific SAR model fit Stortini et al.: Island biogeography in large marine ecosystems 163

Fig. 5. Relationship between pre- 1992 and post-1991 changes in (a) prey and (b) mesopredator alpha diversity and density (mean abundance tow−1). The blue solid line represents the fitted relationship (which was weighted by the product of the standard error of the dif- ferences in jackknife alpha diversity and density between regimes); blue dotted lines represent the error associated with the fitted relationship. Horizontal and verti cal grey dotted lines indicate no change in either alpha diversity (horizontal) or density (vertical). Bank abbreviations as in Fig. 2 was lengthened into the late-1990s for both prey and to post-collapse changes in alpha diversity were mesopredator trophic groups, suggesting a poten- accompanied by changes in density (abundance per tially lagged response of the SAR to predator deple- unit area) on each bank. Increases in prey alpha tion. For the mesopredator group, the strict post-1991 diversity across the banks were positively (and sig- regime was not characterized by significantly higher nificantly) correlated with increases in prey densi- SAR slopes compared to the pre-1992 regime, but a ties, even when the relationship was weighted by the positive temporal trend was evident through both 15 inverse of the product of standard errors associated and 20 yr moving windows (Supplement 7). with these changes (r2 = 0.43, p < 0.05; Fig. 5a). An analysis of finer-scale temporal changes in prey densities and species counts (per year) revealed that pos- Towards a mechanistic understanding of changes itive trends in annual prey species counts were in SAR slope accompanied by, and strongly correlated with (average Pearson r = 0.46, maximum r = 0.66 on Misaine To gain insight into the processes driving observed Bank), positive trends in annual prey densities on the increases in the slope of the prey SAR, and the majority of the banks (Supplement 8). strength of the mesopredator SAR during the post- An analysis of species identities within the prey collapse regime (Fig. 4), we evaluated whether pre- trophic group in each regime revealed that species

Fig. 6. Prey species richness in the (a) pre- 1992 and (b) post-1991 regimes. In the post- 1991 regime, all species previously unobserved on the banks were categorized as the ‘Scotian Shelf (SS) pool’ (those that were observed in deeper, off-bank regions of the Scotian Shelf in the pre-1992 regime), or ‘colonist’ (those that were not observed anywhere on the Scotian Shelf prior to 1991). ‘Core’ species constitute the prey species that were observed on the banks in the pre- collapse regime. On the x-axis, the 10 banks are arranged from the smallest (left) to largest (right). Bank abbreviations as in Fig. 2 164 Mar Ecol Prog Ser 607: 155–169, 2018

that were not observed anywhere on the Scotian Shelf colonists and SS pool species did become common in prior to 1991 were largely responsible for the area- the post-1991 regime, being observed 17 (shorthorn dependent increase in prey alpha diversity in the sculpin Myoxocephalus scorpius) and 24 times post-1991 regime (referred to as ‘colonists,’ Fig. 6; (Atlantic hookear sculpin Artediellus atlanticus) on Supplement 3). The colonists on the western half of some banks. An increase in the strength of the corre- the shelf were made up of species having southern lation between community dissimilarity (given pres- affinities while the eastern half colonists were gener- ence/absence of species) and geographic distance ally composed of species with northern affinities. between banks in the post-1991 era (r2 = 0.31, p < Other contributing species to the post-1991 increases 0.001; Fig. 7a) relative to the pre-1992 era (r2 = 0.03, in alpha diversity originated from deeper habitats p = 0.14), suggested that the origin of colonist and SS on the Scotian Shelf (referred to as ‘SS pool,’ Fig. 6; pool species may have impacted post-1991 prey com- Supplement 3). One prey species (marlin-spike gren - munities, and potentially the re sulting SAR. adier Nezumia bairdii), which was ob served once on The development of a weak SAR in the mesopreda- Western and Banquereau Banks in the pre-1992 era, tor trophic group during the post-1991 regime, as became extirpated from the banks in the post-1991 contrasted to the non-existent SAR in the pre-col- regime (Table S2 in Supplement 3). This is in stark lapse regime (Fig. 4b), is indicative of some level of contrast to the 15 colonist and 11 SS pool species, release from competition following the predator col- which appeared on the banks in the post-1991 lapse. There was no significant correlation (r2 = 0.01, regime (Supplement 3). p = 0.81) between pre- and post-collapse changes in Neither colonists nor SS pool species (together mesopredator alpha diversity and densities (Fig. 5b). referred to as ‘new species’) contributed significantly However, strong positive correlations between annual to the observed increases in prey abundances across mesopredator species counts and densities were the banks (Supplement 9), and most new species observed on Brown’s (Pearson r = 0.63), Western (r = were observed in only 1 to 4 tows per bank during 0.52), La Have (r = 0.75), and Roseway (r = 0.55) the post-1991 period (Table S2). However, some Banks (Supplement 8). Mesopredator species counts and densities remained relatively stable over time across the remaining banks (Supplement 8), with the appearance of only 2 colonist and 2 SS pool mesopredators to the banks in the post- 1991 regime (Supplement 3). The appearance of these 4 new species (2 colonists and 2 SS pool) did not dra- matically contrast the extirpation of 3 mesopredator species (common searo - bin Prionotus carolinus, Artic eelpout Lycodes reticulatus, and offshore hake Merluccius albidus) from the banks in the post-1991 regime (Supplement 3). However, while the extirpated species were observed only once or twice per bank in the pre-1992 era, 1 colonist mesopredator species, Newfoundland eelpout L. terraenovae, was observed 7 times on Misaine Bank in the post-1991 era (Table S3 in Supplement 3). Further investigation of species frequency of occurrence revealed that many mesopredator species with high frequency of occurrence on some Fig. 7. Correlation of (a) prey and (b) mesopredator bank community dissimilarities, given presence and absence of species, and geographic distance (m) banks in the pre-1992 era, and even between bank centroids during pre-1992 (left column) and post-1991 (right higher frequency of occurrence in the column) regimes post-1991 era, appeared on other banks Stortini et al.: Island biogeography in large marine ecosystems 165

where they were previously unobserved in the post- pleted further supported the mechanistic underpin- 1991 regime, reminiscent of a range expansion (e.g. nings of TTIB. Numerous investigations (e.g. Frank & winter skate Leucoraja ocellata, witch flounder Glyp- Brickman 2000, Dulvy et al. 2004) have noted the tocephalus cynoglossus, yellowtail flounder Limanda strong positive correlation between population size ferruginea, little skate Leucoraja erinacea, monkfish and extinction risk. Other determinants of extinction Lophius americanus, and sea raven Hemitripterus risk include geographic range size, habitat alteration, americanus; Table S3). An increase in the strength of responses to exploitation, and life history traits such the correlation between bank mesopredator commu- as age at maturity, body size, life span, and growth nity dissimilarities and geographic distance among rate (Hutchings & Reynolds 2004). An examination of banks in the post-1991 regime (r2 = 0.22, p < 0.001) all potential indicators of extinction risk was beyond relative to the pre-1992 regime (r2 = 0.002, p = 0.67) the scope of this paper. However, the increased den- (Fig. 7) suggests that movement of mesopredator sities of core prey and mesopredator species (both species among banks, or from similar off-bank areas, smaller-bodied and therefore inherently at lower risk contributed to changes in bank mesopredator com- of extinction than large predators; Reynolds et al. munity compositions, and potentially the mesopreda- 2005, Olden et al. 2007) in the post-1991 era, suggests tor SAR, in the post-1991 regime. that extinction risk was diminished. Moreover, in the post-1991 era, many mesopredator species ex hibited increases in their frequency of occurrence on the DISCUSSION banks and an apparent migration from densely populated banks to banks previously unoccupied (Table Our results provide support for the predictions of S3), suggesting that geographic range expansions TTIB across the perturbed submarine banks of the may have also occurred. Shackell & Frank (2003) doc- Scotian Shelf. To our knowledge, this is the first study umented the geographic range expansions of many to find support for TTIB at large spatial scales, in a prey and mesopredator species on the Scotian Shelf marine ecosystem, and for any ecosystem at these after the collapse of large predator populations. Fur- scales. Alpha diversity of prey species increased on ther, Fisher & Frank (2004) found that many of the the banks in the post-predator collapse regime (post- species mentioned above exhibited strong positive 1991), the increase being greatest on the largest correlations between abundance and area occupied, banks. The result was a significant increase in the particularly following predator collapse. We found slope of the SAR for this trophic group (Fig. 4a, that increases in prey densities were strongly and Table 1). Based on TTIB, we also anticipated that the positively correlated with the area-dependent in- collapse of large-bodied predator populations would creases in prey alpha diversity at both regime and an- result in increased alpha diversity and the slopes of nual time scales (Fig. 5a, Supplement 8). Increases in SAR within the mesopredator complex. mesopredator densities and alpha diversity were, in A substantial body of literature details the phenom- contrast, only evident on larger banks (Brown’s and enon of ‘mesopredator release,’ i.e. release from Western; Supplement 8). This implies that different competition and/or predation on juvenile stages, mechanisms governed the changes in SAR of these 2 associated with the depletion of large-bodied pre - trophic groups. For the mesopredator trophic group, dators (Crooks & Soulé 1999, Baum & Worm 2009, in creases in alpha diversity on the largest banks, Prugh et al. 2009). A nearly non-existent SAR during which subsequently led to a strong SAR in the post- the pre-1992 period resulted in a lack of statistical 1991 regime, resulted primarily from a migration of significance in terms of the increase in SAR slope for abundant core species from densely populated banks the mesopredator trophic group in the post-1991 era. to previously unoccupied banks (Table S3). In con- However, the strength (r2) of the relationship more trast, core species in the prey trophic group evidently than quadrupled (Fig. 4b, Table 1), and bank area experienced increases in densities and consequent was the only significant predictor of alpha diversity reductions in extinction risk as a consequence of re- within this trophic group, as it was for the prey duced predation in the post-1992 period, but an ex- trophic group (Supplement 6). We interpret this find- amination of prey species identities in the pre-1992 ing as support for the hypothesis that TTIB may also and post-1991 regimes revealed that increases in spe- apply to mesopredator release in marine ecosystems. cies immigrations onto, and/or successful colonization The finding that increases in prey SAR slope were of the banks also played a sig nificant role in the coincident with reduced extinction rates in core prey steepening of the prey SAR in the post-collapse and mesopredator species when predators were de- regime (Fig. 6). 166 Mar Ecol Prog Ser 607: 155–169, 2018

More than half (58%) of the new prey species had have theorized about how various types and strengths not been reported on the Scotian Shelf prior to 1991 of species interactions, in combination with environ- (i.e. were considered ‘colonists,’ Supplement 3). The mental drivers at different scales, may impact the southern and northern affinities of these species, and scaling of diversity in ecological com munities (Levins the increased correlation of prey community dis - & Culver 1971, Whittaker 2000, Calcagno et al. 2011). similarities and geographic distance among banks It is clear, however, that more empirical evidence di- (Fig. 7a) suggests that these new species immigrated rectly related to the theory of island biogeography, from other regions and may well have successfully and its modern extensions such as the TTIB, is re- colonized the banks due to high productivity and low quired if these theories are to be effectively evaluated. predation pressure. It is not possible to distinguish This study provides the first empirical support for the whether rates of immigration increased, or simply the extension of the TTIB to the scales of large marine frequency of successful colonization. It is possible ecosystems, provides insight into the inter-trophic that immigration of these species (i.e. attempted col- level dynamics of ecosystem change, and contributes onization) to the banks has occurred in the past (at to a more integrative theory of island biogeography what frequency is unknown), but successful colo- (Lomolino 2000, Cazelles et al. 2016). nization was only permitted when conditions became Our findings also contribute support for the grow- favorable (post-1991). It is also possible that some of ing consensus that, despite global-scale declines in these newly detected species were always present on biodiversity (e.g. Butchart et al. 2010), diversity may the banks, but went undetected due to low abun- actually increase at local scales in some regions in dances when predators were present. However, this response to changing ecosystem states (Sax et al. argument is inconsistent with the reality that these 2002, Dornelas et al. 2014, Batt et al. 2017). While one immigrant/colonist species exhibited little to no in - goal of biodiversity conservation is to maintain eco- creasing trend in abundance in the post-collapse re- system resilience, our analyses, among other reveal- gime (Supplement 9). ing studies (e.g. Ellingsen et al. 2015), exposes that Given the limited pre- to post-collapse difference increased alpha diversity may, in itself, be an unreli- in average bottom temperature across the banks able indicator of ecosystem health. Indeed, on the sub - (Supplement 2), it does not appear that the immi- marine banks of the Scotian Shelf, the pronounced grants/colonist species observed post-1992 were re - increase in prey alpha diversity was a symptom of sponding to long-term or local-scale tem perature a disruptive ‘trophic cascade’ (Frank et al. 2005, changes. Moreover, given that none of these small- Ellingsen et al. 2015). This finding is consistent with, bodied species has been commercially exploited (Sup- and supportive of, the increased interest in the large plement 3), their absence from the banks in the pre- fish indicator (Modica et al. 2014), functional diver- collapse regime could not have been due to directed sity (Cadotte et al. 2011), and other ecosystem diag- fishing. It is also possible that as a consequence of nostics, all of which signal a shift in the mindset of relaxed predation and lowered extinction rates post- conservationists from a preoccupation with the pro- 1991, successful prey immigration was facilitated by tection of biodiversity to the protection of diversity these immigrant species seeking refuge amongst other of traits and the function of trophic webs. highly abundant groups as reported by Landeau & Given the strong influence of body size on life his- Terborgh (1986) and Bakun & Cury (1999). We con- tory characteristics, including population stability in clude that reduced extinction rates and increased space and time (Roff 1992, Swain et al. 2007), it has rates of immigration and/or colonization collectively been argued that such an increased dominance of led to the increased slopes of the prey SAR slope in small-bodied species would lead to ecosystem insta- the post-collapse regime, while range expansion and bility (Petrie et al. 2009). This reasoning is not incon- consequent decreases in extinction risk contributed sistent with the increased dependence of prey and to the strengthened mesopre dator SAR. mesopredator alpha diversity on bank area in the Cazelles et al. (2016) recently called for the integra- post-collapse regime (Fig. 4), and the increased oc - tion of a wider range of species interactions into the currence of rare colonist species (Supplement 3), theory of island biogeography. Our findings, as de- both of which suggest that these offshore bank com- tailed above, suggest that inclusion of the interaction munities have become more insular and possibly less between predator abundance and prey immigration/ temporally stable. It is also important to highlight colonization rates, and between predator abundance that the post-1991 increase in prey alpha diversity and mesopredator extinction rates, would be worth- does not discount the potential for a future decline in while additions to the evolving TTIB. Many researchers alpha diversity at all trophic levels and body sizes, Stortini et al.: Island biogeography in large marine ecosystems 167

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Editorial responsibility: Jake Rice, Submitted: May 31, 2018; Accepted: October 25, 2018 Ottawa, Ontario, Canada Proofs received from author(s): November 30, 2018