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Manuscript Number: Title: Maximising reserve design efficiency when resources are limited: terrestrial reserves inclusive of marine ecological value for a forestnesting seabird Article Type: Full Length Article Keywords: Marbled Murrelet; reserve design; efficiency; terrestrial and marine habitat; conservation planning Corresponding Author: Dr. Stephanie Lynn Hazlitt, Ph.D. Corresponding Author's Institution: University of British Columbia First Author: Stephanie Lynn Hazlitt, Ph.D. Order of Authors: Stephanie Lynn Hazlitt, Ph.D.; Tara G Martin; Laura Sampson; Peter Arcese Abstract: Advances in conservation planning theory have promoted a more systematic approach to locating and designing reserve systems, to improve efficiency of limited conservation resources and to increase the likelihood that established reserves or reserve systems will actually promote the persistence and long-term survival of species and/or ecosystems. We used the marbled murrelet, an old-growth nesting seabird, as a case study to explore methods of incorporating multiple measures of ecological value into the spatial reserve design process. We used the cost function within the spatial reserve design algorithm in Marxan as a measure of ecological value, and identify solutions for the spatial design of marbled murrelet nesting habitat reserves with and without the inclusion of marine foraging habitat information. The inclusion of marine habitat value altered the near-optimal terrestrial reserve design modestly to dramatically, depending on the overall conservation target, the proportion of the conservation target captured in pre-existing reserves, and the weighting or influence of marine habitat value used in the total measure of ecological value. Including marine habitat value had a substantial influence on the resulting terrestrial reserve design when the terrestrial habitat target was low and when little or none of the target was represented in pre-existing protected areas. Based on these results, including marine habitat value should increase terrestrial reserve design efficiency most in regions where there are still substantial areas of terrestrial nesting habitat potentially available, where reserve designs are relatively unconstrained by pre-existing reserve systems and when resources are insufficient to protect the majority of available habitat. Incorporating marine foraging habitat value should create efficiencies in terrestrial reserve selection by maximizing the reproductive and survival value of forest habitat reserves for nesting marbled murrelets, increasing the likelihood that marbled

murrelet populations persist on the landscape and/or hastening species recovery. This paper presents a novel framework for incorporating multiple measures of ecological value within the spatial reserve design process, a technique that could be used to increase reserve design efficiencies when resources are limited and species or populations are influenced by events across multiple landscapes.

Cover Letter

Dr. Richard B. Primack Editor-in-Chief, Biological Conservation Biology Department Boston University 5 Cummington Street Boston, MA 02215 USA 20 July 2009 Dear Dr. Primack, We wish to submit the manuscript Maximising reserve design efficiency when resources are limited: terrestrial reserves inclusive of marine ecological value for a forest-nesting seabird for publication as a research paper in Biological Conservation. Our paper presents a novel framework for incorporating multiple measures of ecological value within the spatial reserve design process, a technique that could be used to increase the efficiency of reserve designs when conservation resources are limited. This work has broad applicability to topics in systematic conservation planning, species and ecosystem conservation and resource management. We feel that Biological Conservation is an appropriate medium to present this study, and that the subject material would be familiar and of interest to your readership. The original material presented in this manuscript has not been published or submitted, in whole or in part, for publication elsewhere, and all authors consent to the submission. In addition, all sources of funding and any research discussed but not carried out by the authors have been appropriately acknowledged. We appreciate your consideration of our manuscript for publication in Biological Conservation. I can be contacted by telephone +1 604 827 5843, cell +1 250 516 0390 or by e-mail at stephanie.hazlitt@ubc.ca. Sincerely,

Dr. Stephanie L. Hazlitt Centre for Applied Conservation Research Department of Forest Sciences University of British Columbia Vancouver, BC V6T 1Z4 Canada cc Tara G. Martin, Laura Sampson, and Peter Arcese, coauthors

* Manuscript

Maximising reserve design efficiency when resources are limited: terrestrial reserves inclusive of marine ecological value for a forest-nesting seabird

Stephanie L. Hazlitt1*, Tara G. Martin1,2, Laura Sampson1, and Peter Arcese1

Centre for Applied Conservation Research, Department of Forest Sciences, University of British Columbia, 2424 Main Mall, Vancouver, British Columbia, Canada V6T 1Z4
2

CSIRO Sustainable Ecosystems, 306 Carmody Road, St Lucia, Queensland 4067 Australia

Corresponding author: Stephanie L. Hazlitt Centre for Applied Conservation Research, Department of Forest Sciences, University of British Columbia, 2424 Main Mall, Vancouver, British Columbia, Canada V6T 1Z4 Telephone: +1 604 827 5843 Fax: +1 604 822 9102 E-mail: stephanie.hazlitt@ubc.ca

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Abstract Advances in conservation planning theory have promoted a more systematic approach to locating and designing reserve systems, to improve efficiency of limited conservation resources and to increase the likelihood that established reserves or reserve systems will actually promote the persistence and long-term survival of species and/or ecosystems. We used the marbled murrelet, an old-growth nesting seabird, as a case study to explore methods of incorporating multiple measures of ecological value into the spatial reserve design process. We used the cost function within the spatial reserve design algorithm in Marxan as a measure of ecological value, and identify solutions for the spatial design of marbled murrelet nesting habitat reserves with and without the inclusion of marine foraging habitat information. The inclusion of marine habitat value altered the near-optimal terrestrial reserve design modestly to dramatically, depending on the overall conservation target, the proportion of the conservation target captured in pre-existing reserves, and the weighting or influence of marine habitat value used in the total measure of ecological value. Including marine habitat value had a substantial influence on the resulting terrestrial reserve design when the terrestrial habitat target was low and when little or none of the target was represented in pre-existing protected areas. Based on these results, including marine habitat value should increase terrestrial reserve design efficiency most in regions where there are still substantial areas of terrestrial nesting habitat potentially available, where reserve designs are relatively unconstrained by pre-existing reserve systems and when resources are insufficient to protect the majority of available habitat. Incorporating marine foraging habitat value should create efficiencies in terrestrial reserve selection by maximizing the reproductive and survival value of forest habitat reserves for nesting marbled murrelets, increasing the likelihood that marbled murrelet populations persist on the landscape and/or hastening species recovery. This paper presents a novel framework for incorporating multiple measures of ecological value within the spatial reserve design process, a technique that could be used to increase reserve design efficiencies when resources are limited and species or populations are influenced by events across multiple landscapes.

Keywords: Marbled Murrelet, reserve design, efficiency, terrestrial and marine habitat, conservation planning

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1. Introduction The establishment of reserves for the maintenance of biodiversity values is one of the cornerstones of regional conservation strategies, with the primary goal of separating biodiversity from processes that threaten species or ecosystems in the wild (Margules and Pressey, 2000). Advances in conservation planning theory have promoted a more systematic approach to locating and designing reserve systems, aided by the development of mathematical site-selection algorithms that guide the identification of priority areas (e.g., Ball and Possingham, 2000; Cameron et al., 2008; Margules and Pressey, 2000; Wilson et al., 2007). The primary drivers of a more systematic approach include improved efficiency of limited conservation resources and an increased likelihood that established reserves or reserve systems will actually promote the persistence and long-term survival of species and/or ecosystems (e.g., Cameron et al., 2008; Margules and Pressey, 2000; Martin et al., 2007; McDonald-Madden et al., 2008; Wilson et al., 2007). Recent efforts have examined methods to optimize planning for multiple species (e.g., Nicholson et al., 2006), or for taxa that are influenced by events across multiple jurisdictions (e.g., migratory birds, Martin et al., 2007). Here, we extend these methods to incorporate multiple measures of ecological value within the spatial reserve design process, using the Marbled Murrelet (Brachyramphus marmoratus), a small seabird which requires old-growth forests in which to nest and high quality marine habitats in which to forage, as a case study. Marbled murrelets live along the northern Pacific Coast of North America, spending approximately 90% of their time in marine waters, but come on-shore during the spring and summer to breed. Marbled murrelets in British Columbia nest primarily on the moss-covered branches of old-growth conifers, up to 50 km inland but mostly within 30 km from the shoreline (Burger, 2002; Ralph et al., 1995). The Canadian population of marbled murrelets was assessed as Threatened in 1990 by the Committee on the Status of Endangered Wildlife in Canada, based on estimated declines in murrelet nesting habitat in coastal old-growth forests, resulting in their listing under the federal Species at Risk Act (Threatened, Schedule 1, 2003). However, in addition to declines in terrestrial nesting habitat, many recent studies suggest that the quality of near-shore marine habitat and availability of high quality forage fish can also affect the breeding success of marbled murrelets, and that access to these resources is likely to be an important factor for influencing the growth and potential recovery of marbled murrelet populations (e.g., Becker and Beissinger, 2006; Becker et al., 2007; Beissinger and Peery, 2007; Norris et al., 2007; Peery et al., 2004; Ronconi, 2008). Many jurisdictions are implementing conservation plans for the protection and management of marbled murrelet old-growth nesting habitat (e.g., Raphael, 2006). For example, the province of British Columbia is establishing old-growth reserve areas as part of a land use planning and ecosystem-based management process, to protect old-growth coastal temperate rainforest habitats in a roughly 6.4 million hectare planning region. Although preliminary research suggests that the proximity of old-growth nest sites to productive marine areas may affect the potential quality of nesting habitat to marbled murrelets (e.g., Becker and Beissinger, 2003; Ronconi, 2008; Yen et al., 2004), empirical data on marbled murrelet marine foraging habitat use and the 3

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identification of marine hot spots are scarce. As a result, conservation initiatives for marbled murrelets have focused on the selection of high quality terrestrial habitat, but ignored the fact that nesting habitat will vary in its proximity to marine foraging areas likely to support the requirements of adult murrelets during the pre-breeding and nesting stage, or the requirements of fledglings, which forage independently after leaving the nest. In contrast, much recent research indicates that several reliable near-shore predictors of high quality, marbled murrelet breeding foraging habitat exist, based on studies of species distribution, foraging success (e.g., Burger et al., 2008; Kuletz, 2005; Miller et al., 2002; Ronconi, 2008; Yen et al., 2004) and employing radio-telemetry (Barrett, 2008; Kuletz, 2005). For example, marbled murrelets consistently forage within 2 km of the terrestrial shoreline, usually within 500m (Burger et al., 2008; Day et al., 2003; Ronconi, 2008). Marbled murrelets also prefer to forage in shallow water, c 20 - 30 m deep, and rarely deeper than 50 m (Burger et al., 2008; Day et al., 2003; Kuletz, 2005; Ronconi, 2008). Distance from sandy beaches or substrates has also proved to be a useful predictor of murrelet foraging activity (e.g., less than 1 km, Ronconi, 2008; Yen et al., 2004), presumably due to the strong association between the presence of sandy substrates and forage fishes such as the sand lance (Ammodytes hexapterus), a common murrelet prey item (Haynes et al., 2007; Ostrand et al., 2005; Ronconi, 2008). Other predictors of murrelet foraging habitat during breeding include oceanographic variables such as sea surface temperature and salinity (Barrett, 2008; Ronconi, 2008; Yen et al., 2004), but because these attributes vary spatially and temporally, employing them as spatial predicators of foraging habitat suitability is challenging (Barrett, 2008). The goal of this paper was to explore methods to optimize the spatial distribution of marbled murrelet terrestrial nesting habitat with respect to features in the marine environment likely to indicate high quality foraging sites for breeding birds. In particular, we demonstrate how nearshore marine predictors, such as proximity to shoreline and water depth (e.g., Burger et al., 2008), can be used to document the consequences of emphasizing marine foraging values in algorithms designed to identify near-optimal terrestrial reserve designs for marbled murrelets. To do so, we identified solutions for the spatial design of marbled murrelet nesting habitat reserves with and without the inclusion of marine foraging habitat information, and then determined how similar terrestrial reserve designs, selected via a conventional emphasis on terrestrial values, are to those selected with the addition of marine habitat value assumptions. As a result, our paper presents a novel framework for incorporating multiple measures of ecological value within the spatial reserve design process, a technique that could be used to increase the efficiency of reserve design when resources are limited and/or when species or populations are influenced by events across multiple landscapes.

2. Methods 2.1 Study region and terrestrial reserve design 4

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We focused our study on the south-central coastal region of British Columbia (Figure 1). We employed ArcMap 9.2 (ESRI) and MARXAN v.1.8 to conduct spatial reserve design simulations (Ball and Possingham, 2000). Using the repeating shapes tool (Jenness Enterprises; http://www.jennessent.com/arcgis/repeat_shapes.htm) we created 17,479 hexagonal planning units (PUs) of 100ha in size over the entire terrestrial study area. Terrestrial data included the distribution and amount of suitable murrelet nesting habitat (Mather et al., 2005) and spatial boundaries of existing protected areas (e.g., parks and protected areas, conservancies, wildlife habitat areas, downloaded from the BC Land and Resource Data Warehouse) (Figure 1). The total area of marbled murrelet terrestrial nesting habitat within each terrestrial hexagon PU and the amount of terrestrial nesting habitat already captured by existing protected areas within each terrestrial hexagon PU was calculated using the polygon in polygon analysis in Hawths tools (http://www.spatialecology.com/htools/tooldesc.php). For one set of reserve scenarios we locked into the reserve solution all marbled murrelet habitat already within protected areas (14,318.7 ha). We did this by locking in all PUs that contained marbled murrelet habitat where 70% or more of that habitat was contained within an existing protected area. Spatial reserve design simulations were conducted using MARXAN where each scenario included 100 runs, using simulated annealing with normal iterative improvement, and 1,000,000 iterations per run with 10,000 temperature decreases. We used an irremovable boundary file (Game and Grantham, 2008), created using JNCC ArcGIS extentions (available at http://www.uq.edu.au/marxan), although no boundary length modifier was used because murrelets often fly long distances between marine and terrestrial habitats and little is known about limits to forest patch size use for nesting (Burger, 2002). We utilized an estimate of terrestrial ecological value for each PU as the cost parameter in each reserve design scenario (Ardron et al., 2008; Game and Grantham, 2008). The terrestrial planning unit cost was based on terrestrial ecological value, calculated as (1 (amount of terrestrial habitat within PU)/(maximum amount of habitat among PUs))*100. The terrestrial PUs with the highest ecological value had the lowest cost to the MARXAN solution, and were thus selected preferentially during the reserve design process. We ran MARXAN with a single target, where the emphasis on ecological value was denoted through the cost, ranging from 0 (highest ecological value) to 100 (no ecological value), with the species penalty factor set to 100. Reserve habitat targets are summarized in Table 1. Briefly, we created example terrestrial reserve scenarios based on 3 hypothetical targets, protecting 70%, 50% and 30% of existing terrestrial marbled murrelet nesting habitat (179,466 ha). Using a range of targets allowed us to explore the impact of changing levels of protection while including or excluding specific marine features in the reserve design process. However, these scenarios and the resulting reserves are not intended as indicators or as an analysis regarding targets for marbled murrelet terrestrial habitat conservation. The Canadian Marbled Murrelet Recovery Team (CMMRT) has recommended the protection of 70% of suitable 2002 terrestrial nesting habitat within each 5

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coastal marbled murrelet conservation area (CMMRT, 2003). Targets of 50% and 30% of existing habitat correspond to the results of population viability analyses of British Columbia marbled murrelet populations, which recommend maintaining a minimum of 12 000 breeding pairs (36 000 birds) distributed in three to six management regions (Steventon et al., 2003, 2006). Maintaining a breeding population of this size would require from 600,000 to 1.2 million ha of suitable habitat coast-wide, assuming a density of 0.02 or 0.01 birds/ha, or 100,000 to 200,000 ha per each of the six CMMRT suggested conservation regions (Steventon et al., 2006). Because the south-central coast study region is approximately one half of the central mainland coast CMMRT conservation area (CMMRT, 2003); targets identified via analyses of population viability imply that a minimum of approximately 30% to 50% of the remaining suitable habitat (50,000 to 100,000 ha of habitat, depending on the predicted density) in the south central coast is required to maintain viable murrelet populations in future, although abundance would be substantially reduced from historical population levels (Steventon et al., 2006). 2.2 Marbled murrelet breeding season marine foraging habitat We used the literature to create maps of potentially suitable marbled murrelet foraging habitat during the breeding period, based on consistent predictors of marbled murrelet marine distribution and marine foraging areas identified during breeding and reported in independent research studies (Table 2 and references therein). Maps were created by first establishing a layer of 10 ha marine hexagons (n = 36,054, http://www.jennessent.com/arcgis/repeat_shapes.htm) covering the entire marine portion of the study area to a distance of < 5km from shore (see Burger et al., 2008). We derived information for each consistent near-shore predictor (e.g., distance from shoreline, shoreline and substrate type, and depth; see Table 2) using tools in ArcMap 9.2. We used the same shoreline classification data as Ronconi (2008) and Barrett (2008) from the Integrated Land and Management Bureaus Physical and Biophysical Shorezone Mapping System. The linear amount of sandy beach within a 2km buffer around each marine hexagon was summed, following the same classifications outlined by Ronconi (2008; Classes 24: sand/gravel flats; 27: wide sand beach 28: sand flat; and 30: narrow sand beach from the Biophysical Shorezone Mapping Classification System), which are considered to indicate likely sand lance habitat (Haynes et al., 2007). Distances from each marine PU centre to the nearest sandy beach and to the terrestrial shoreline were calculated using the proximity tool in ArcMap 9.2. Each 10 ha marine hexagon was ranked according to its potential as suitable murrelet foraging habitat, based on 5 different sets of assumptions about the marine features likely to be most influential on murrelet foraging success. These were: M1 Distance to terrestrial shoreline: > 2km from shore = 0, 500m to 2km = 1 and 500m = 2; M2 Depth: > 50m = 0, 20m to 50m = 1 and < 20m = 2; M3 Distance to nearest sandy shoreline: > 500m = 0, 500m = 1; M4 Amount of sandy shoreline within a 2km buffer: 0 = 0, 1000m = 1, >1000m = 2; M5 Simple

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marbled murrelet marine foraging habitat model: M1 score +M2 score + M4 score. Finally, a spatial layer was created to record polygon scores for each marine model (M1-5; Table 2). 2.3 Incorporating marine foraging habitat value and terrestrial habitat value The area of each marine habitat class, for each marine model (M1-5), was calculated within a 30km buffer around each terrestrial planning unit. For each marine model, the total weighted value of marine habitat quality for each terrestrial planning unit was calculated as: area of score 1 + (area of score 2 x 2) + (area of score 3 x 3) + (area score n x n) for each marine model (M1-5). A measure of marine ecological value was calculated for each terrestrial planning unit using the same formula as for terrestrial value: (1 (weighted amount of marine habitat within 30 km radius of PU)/(maximum amount of weighted amount of marine habitat within 30 km radius of PUs))*100 for each of the marine models M1 through M5. To determine the impact of considering marine habitat value in terrestrial reserve design we again employed the cost function in MARXAN, by weighting marine and terrestrial habitat quality models equally ((marine value for each model)(0.5)+(terrestrial value)(0.5)). As in the previous analysis, the terrestrial PUs with the highest combined ecological value scores had the lowest cost to the MARXAN solution, and were thus selected preferentially during the reserve design process. 2.4 Comparison of reserve solutions We examined two kinds of reserve design outputs, the best solution and a sum of all near optimal solutions, hereafter called the summed solution (Ball and Possingham, 2000; Game and Grantham, 2008). The best reserve solution is the solution with the best objective value or the most efficient solution out of all the runs (e.g., meeting the biodiversity targets with the lowest cost), however it is important to note that the best solution may only be marginally better than numerous other solutions (Game and Grantham, 2008). The summed solution provides the selection frequency of each planning unit across all of the runs (n = 100), providing an indication of how useful each of the planning units is for deriving an efficient reserve design or which of the planning units are priorities for the reserve design (Game and Grantham, 2008). We compared our terrestrial reserve solution for the three marbled murrelet habitat targets, with and without locked-in pre-existing reserves, to each of six resulting reserves similarly derived in MARXAN, but based on an equal weighting of marine and terrestrial habitat values. The first comparison involved a reserve design using a terrestrial value-only cost model, but excluding terrestrial habitat > 30km from the nearest saltwater shoreline, reflecting recent evidence that most marbled murrelets in BC nest within 30km from the shoreline (D. Lank, Simon Fraser University, unpublished data, Burger, 2002; Kuletz, 2005). The next five comparisons were conducted giving equal weight to terrestrial and marine ecological value as estimated for each of five derived marine habitat models (M1-5; Table 2). Resulting spatial reserve designs were compared using the kappa coefficient (for best solutions, Jensen, 1996) and correlation analyses (for summed solutions, Ardron et al., 2008). Finally, to explore the relative influence of emphasizing terrestrial versus marine habitat values in terrestrial reserve designs for murrelets, 7

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we also compared the summed solutions for terrestrial murrelet reserves across 3 habitat targets (but excluding locked-in pre-existing reserves) to reserve designs constructed by incrementally increasing by 10% our emphasis on marine (M5 model) versus terrestrial habitat values, ending with a terrestrial reserve in which proximity to high quality marine habitat was given 100% emphasis over terrestrial habitat values.

3. Results We compared the best and summed reserve solutions for three marbled murrelet terrestrial habitat targets (30, 50 and 70%; Table 1), with and without locked-in pre-existing reserves, based solely on terrestrial habitat value with solutions that also included marine habitat values. Our assumptions about marine habitat values followed two sets of scenarios; the first excluded all nesting habitat > 30km from the sea from the solution. The second were based on 5 marine habitat value attributes or sets of attributes (Table 2) given equal weight to terrestrial and marine values in the reserve selection process (Figures 2 and 3). We also explored the influence of marine habitat value in terrestrial reserve design by examining the summed solutions of a series of reserves, based first solely on terrestrial habitat value (marine weight = 0), and then by incrementally increasing our weightings of marine relative to terrestrial habitat values (Figure 4). Best and summed reserve similarity was highest between terrestrial and terrestrial plus marine value when the habitat target was high (70%: 66-67% best; 98% summed) compared to the lowest target (30%: 53-57% best; 90-93% summed; Figures 2 and 3). Terrestrial reserves were most similar to the scenario with nesting habitat > 30km from the sea excluded for both the best and summed solutions, with little variation among the three target scenarios for that comparison (63-67% best; 98-99% summed; Figures 2 and 3). Reserve similarity was always higher for each target scenario when pre-existing reserves were locked-in to the solution, for both best and summed solutions (Figures 2 and 3). However, the most similar best solutions occurred when the proportion of locked-in pre-existing reserves represented a larger fraction of the final solution, which occurred as the target for nesting habitat was reduced from 70 to 30% (30%: 77-80%; 50%: 72-76; 70%: 71-72; Table 1, Figure 2). In general, similarity between terrestrial and terrestrial plus marine scenarios differed least when distance to saltwater (excluding terrestrial habitat > 30km from sea) was the only marine value represented (63-67% best; 99-100% summed), and differed most when the relative amount of sandy shoreline within a 2km radius of marine habitat was used to represent favourable foraging habitat (M4: 53-66% best; 90-98% summed; Figures 2 and 3). However, the differences among the terrestrial-only design and the terrestrial plus marine habitat designs were generally quite similar across the five marine habitat quality assumptions (Table 2, Figures 2 and 3). Best reserves influenced by marine values with pre-existing reserves locked-in differed only modestly from the terrestrial-only design (71-80%; Figure 2), and with very little difference among summed solutions (96-99%; Figure 3). In comparison, unlocking pre-existing reserves permitted 8

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a wider range of marine-influenced designs, and resulted in some best solutions differing by up to 47%, and summed solutions differing by up to 10% from comparable designs based only on terrestrial habitat values (30% target scenarios; Figures 2 and 3). The weight or relative ecological importance of marine habitat value compared to terrestrial habitat value had a marked influence on the optimal placement of terrestrial reserves, particularly when the terrestrial habitat target was low (Figure 3). The common fraction of terrestrial polygons chosen in each of three habitat conservation scenarios declined dramatically as an increasing function of the emphasis placed on marine versus terrestrial values in the habitat selection process (Figure 4). This decline was most pronounced with a 30% habitat reservation target, with similarity of the resulting terrestrial-only reserves and terrestrial plus marine habitat value reserves declining to 58% (30%; Figure 4). Similar but less pronounced trends were evident for the scenarios with higher targets for habitat reservation (Figure 4). These patterns arose because, as targets for the reservation of existing habitat were increased, the resulting scenarios included a higher fraction of all available marbled murrelet terrestrial nesting habitat, leaving less room for variation in reserve design.

4. Discussion Marbled murrelet terrestrial habitat reserve selection algorithms that included marine habitat values resulted in modestly to dramatically different reserve designs as compared to those based solely on terrestrial nesting habitat value. The magnitude of the variation depended on the conservation target, the proportion of the conservation target already captured in locked-in preexisting reserves, and the weighting or amount of marine habitat value compared to terrestrial habitat value used in the combined ecological value measure. Comparisons across different habitat target levels, with and without locking in pre-existing reserves, suggests that high conservation targets, relative to what is available in the planning area, and locked-in pre-existing reserves constrain the arrangement of final reserve designs. Final reserves were particularly constrained when pre-existing reserves comprised a large fraction of the total budget for habitat conservation. However, including marine habitat value had a substantial influence on the resulting terrestrial reserve design when the terrestrial habitat target was low and when little or none of the target was represented in pre-existing protected areas (Figures 2 and 3). Marine habitat value also influenced terrestrial reserve designs more strongly as the relative weight of marine versus terrestrial habitat value was increased, particularly when terrestrial habitat targets were low relative to the total area of habitat available in the planning area (Figure 4). As habitat targets were increased, it became more likely that terrestrial habitat in proximity to high value marine habitat was captured in any reserve design scenario, thus reducing the influence of marine foraging habitat as a factor affecting reserve design (Figures 2 and 3). The 9

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reality of most conservation planning exercises, however, is that budgets for conservation are limited and decisions are often made about which habitats to conserve when protection is afforded to only a fraction of currently existing habitat (e.g., Bottrill et al., 2009; Wilson et al., 2006). Our results suggest that the influence of including marine habitat values in terrestrial reserve designs for marbled murrelets will increase where the amount of potential habitat to be reserved is low relative to what exists within the planning area. Currently, these conditions seem most likely to exist in coastal British Columbia and Alaska (CMMRT, 2003). In contrast, marine habitat values are less likely to influence terrestrial reserve design where potential nesting habitat for marbled murrelets is scarce, as in the Georgia Basin of British Columbia (CMMRT, 2003), Washington, Oregon and California (Peery et al., 2004; Piatt et al., 2007). In these areas marine values may, nevertheless, be useful in identifying areas for forest and nesting habitat regeneration. Including marine habitat value in terrestrial nesting habitat reserve designs for marbled murrelets depends on several assumptions about how well particular marine features predict the quality of murrelet foraging habitat (Table 2). Although much evidence now suggests that spatial and temporal variation in marine habitat quality, as well as long-term declines in marine habitat quality, can both affect survival and reproductive success in marbled murrelets (e.g., Becker and Beissinger, 2006; Becker et al., 2007; Beissinger and Peery, 2007; Norris et al., 2007; Peery et al., 2004; Ronconi, 2008), it has yet to be shown that marbled murrelets that nest in proximity to high quality marine foraging areas survive and reproduce better on average than those nesting adjacent to poor or degraded marine habitats. It has also not been shown that marbled murrelet nesting density varies as a function of marine habitat quality. However, there also appears to be little risk in assuming that marine features shown to be favoured by marbled murrelets could be used by managers wishing to estimate the potential value of adjacent marine habitat (e.g., sandy substrates, water depth; Table 2), particularly when alternative terrestrial reserve designs are being considered as part of operational or strategic conservation planning. Empirical data on the use of particular marine foraging areas or distributions of hot spots for foraging marbled murrelets are scarce over the species range (CMMRT, 2003), and we therefore based our theoretical planning exercise on near-shore marine predictors (e.g., Barrett, 2008; Ronconi, 2008; Yen et al., 2004). Although several recent studies have independently arrived at similar suites of near-shore marine predictors of marbled murrelet foraging habitat, two approaches could be taken to further validate these assumptions. First, researchers could document, via marine surveys, the spatial differences in the distribution and density of marbled murrelets during the breeding period and compare those distributions to predictions based on simple (e.g., Table 2) or sophisticated models of marine habitat quality (Yen et al., 2004). Second, surveys of juvenile:adult ratios at-sea could also be compared to predictions about marine habitat quality to test if the apparent reproductive success or survival is higher among birds with unlimited access to high quality marine habitat (techniques described in Kuletz, 2005; 10

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Ronconi, 2008). Both approaches offer a relatively simple means of testing further the hypothesis that consistent differences in marine habitat quality exist and are capable of influencing the demography or terrestrial nesting density in marbled murrelets. Evidence compiled to date suggests that such differences exist and affect the population demography of marbled murrelets in British Columbia and California (e.g., Becker and Beissinger, 2006; Becker et al., 2007; Beissinger and Peery, 2007; Norris et al., 2007; Peery et al., 2004; Ronconi, 2008). Currently, marbled murrelet nesting density is assumed to be equal across all suitable terrestrial nesting habitat in British Columbia (CMMRT, 2003). However, even modest variation in population fitness or terrestrial nesting density as a result of the spatial distribution of marine foraging habitat should create opportunities to achieve efficiency in reserve design if it allows managers to target landscapes likely to hold high densities of marbled murrelets or productive sub-populations. New methods for identifying terrestrial habitat quality, preference and variation in nesting density are being tested (Burger and Waterhouse, 2009; Waterhouse et al., 2008). Utilizing and refining existing knowledge on spatial variation in marine and terrestrial habitat quality should promote more efficient reserves when conservation budgets are limited. Such ecologically efficient approaches to reserve selection might be considered as an alternative to the current approach of maximizing nesting habitat area, with a goal of preferentially protecting high-value habitat but likely protecting less habitat overall. Such offsetting strategies are emerging in the conservation literature (e.g., Wilcox and Donlan, 2007); while controversial, these strategies attempt to increase conservation gains given limited conservation resources. The inclusion of marine habitat values in our simulations resulted in a more efficient terrestrial reserve design for marbled murrelets in the south-central coast of British Columbia, depending on the overall conservation target and pre-existing reserve system. Incorporating marine foraging habitat value should create efficiencies in terrestrial reserve selection by maximizing the reproductive and survival value of forest habitat reserves for nesting marbled murrelets, increasing the likelihood that marbled murrelet populations persist on the landscape and/or hastening species recovery. Our paper presents a novel framework for incorporating multiple measures of ecological or habitat value using the cost function within a spatial reserve design algorithm (MARXAN, Ball and Possingham, 2000). This technique can be used to increase the efficiency of reserve design wherever resources are limited and valued species or populations are influenced by life history events across multiple landscapes.

Acknowledgements We thank the Ecosystem Based Management Working Group, C. Rumsey, H. Horn, A. Burger, L. Waterhouse, S. Gergel, D. Sigg, D. Lank, J. Barrett and 22 attendees at an FIA-FSP funded workshop on marine influences on marbled murrelets for advice and discussions. Funding for this project was provided from an FSP-FIA grant to PA (Y092238), and postdoctoral fellowships to SLH and TGM from NSERC and the Killam Family Trust. 11

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Sand Lance (Ammodytes hexapterus) in the shallow subtidal region of southwestern Vancouver Island. Northwestern Naturalist 88, 155-167.
Jensen, J.R., 1996. Introductory Digital Image Processing: A remote sensing perspective, 2nd Edition. Prentice Hall: Upper Saddle River, New Jersey. Kuletz, K.J., 2005. Foraging behavior and productivity of a non-colonial seabird, the marbled murrelet (Brachyramphus marmoratus), relative to prey and habitat. PhD Thesis, University of Victoria, Canada. Margules, C.R., Pressey, R.L., 2000. Systematic conservation planning. Nature 405, 243-253. Martin, T.G., Chades, I.C., Arcese, P., Marra, P.P., Possingham, H.P., Norris, D.R., 2007. Optimal conservation of migratory species. PLoS ONE 2(8), e751. Mather, M.J., Duncan, J., Woods, S., Guy, S., Blight, L., Stevens, V., Hoyt, J., Hirner, D., 2005. British Columbia Coastal Marbled Murrelet Habitat Suitability Model. British Columbia Ministry of Environment, unpublished report. McDonald-Madden, E., Baxter, P.W.J., Possingham, H.P., 2008. Making robust decisions for conservation with restricted money and knowledge. Journal of Applied Ecology 45, 1630-1638. Miller, S.L., Meyer, C.B., Ralph, C.J., 2002. Land and seascape patterns associated with marbled murrelet abundance offshore. Waterbirds 25, 100-108. Nicholson, E., Westphal, M.I., Frank, K., Rochester, W.A., Pressey, R.L., Lindenmayer, D.B., Possingham, H.P., 2006. A new method for conservation planning for the persistence of multiple species. Ecology Letters 9, 1049-1060. Norris, D.R., Arcese, P., Preikshot, D., Bertram, D.F., Kyser, T.K., 2007. Diet reconstruction and historic population dynamics in a threatened seabird. Journal of Applied Ecology 44, 875-884. Ostrand, W.D., Gotthardt, T.A., Howlin, S., Robards, M.D., 2005. Habitat selection models for Pacific sand lance (Ammodytes hexapterus) in Prince William Sound, Alaska Northwestern Naturalist 86, 131-143. Peery, M.Z., Beissinger, S.R., Newman, S.H., Burkett, E.B., Williams, T.D., 2004. Applying the declining population paradigm: Diagnosing causes of poor reproduction in the marbled murrelet. Conservation Biology 18, 1088-1098. Piatt, J.F., Kuletz, K.J., Burger, A.E., Hatch, S.A., Friesen, V.L., Birt, T.P., Arimitsu, M.L., Drew, G.S., Harding, A.M., Bixler, K.S., 2007. Status review of the marbled murrelet (Brachyramphus marmoratus) in Alaska and British Columbia. U.S.Geological Survey OpenFile Report 2006-1387, Reston, Virginia, USA. Ralph, C.J., Hunt Jr., G.L., Raphael, M.G., Piatt, J.F., 1995. Ecology and conservation of the Marbled Murrelet in North America: an overview, In Ecology and conservation of the marbled murrelet. eds C.J. Ralph, G.L. Hunt Jr., M.G. Raphael, J.F. Piatt, pp. 3-22. USDA Forest Service General Technical Report PSW-152, Albany, California, USA. Raphael, M.G., 2006. Conservation of the marbled murrelet under the northwest forest plan. Conservation Biology 20, 297-305. Robards, M.D., Piatt, J.F., 1999. Biology of the genus Ammodytes, the sand lances, In Sand lance: A review of biology and predator relations and annotated bibliography. eds M.D. Robards, M.F. Willson, R.H. Armstrong, J.F. Piatt, pp. 1-16. USDA Forest Service Research Paper PNWRP-521, Portland, Oregon, USA. Ronconi, R.A., 2008. Patterns and processes of marine habitat selection: foraging ecology, competition and coexistence among coastal seabirds. PhD Thesis, University of Victoria, Canada. 13

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Steventon, J.D., Sutherland, G.D., Arcese, P., 2003. Long-term Risks to Marbled Murrelet (Brachyramphus marmoratus) Populations: Assessing Alternative Forest Management Policies in Coastal British Columbia. Technical Report 012. Research Branch, British Columbia Ministry of Forests, Victoria, British Columbia. Steventon, J.D., Sutherland, G.D., Arcese, P., 2006. A population-viability-based risk assessment of Marbled Murrelet nesting habitat policy in British Columbia. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 36, 3075-3086. Waterhouse, F.L., Donaldson, A., Lank, D.B., Ott, P.K., Krebs, E.A., 2008. Using air photos to interpret quality of Marbled Murrelet nesting habitat in south coastal British Columbia. BC Journal of Ecosystems and Management 9, 17-37. Wilcox, C., Donlan, C.J., 2007. Compensatory mitigation as a solution to fisheries bycatchbiodiversity conservation conflicts. Frontiers in Ecology and the Environment 5, 325-331. Wilson, K.A., McBride, M.F., Bode, M., Possingham, H.P., 2006. Prioritizing global conservation efforts. Nature 440, 337-340. Wilson, K.A., Underwood, E.C., Morrison, S.A., Klausmeyer, K.R., Murdoch, W.W., Reyers, B., Wardell-Johnson, G., Marquet, P.A., Rundel, P.W., McBride, M.F., Pressey, R.L., Bode, M., Hoekstra, J.M., Andelman, S., Looker, M., Rondinini, C., Kareiva, P., Shaw, M.R., Possingham, H.P., 2007. Conserving biodiversity efficiently: What to do, where, and when. Plos Biology 5, 1850-1861. Yen, P.P.W., Huettmann, F., Cooke, F., 2004. A large-scale model for the at-sea distribution and abundance of Marbled Murrelets (Brachyramphus marmoratus) during the breeding season in coastal British Columbia, Canada. Ecological Modelling 171, 395-413.

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Table 1. Marbled murrelet reserve design targets. The target is the proportion of suitable marbled murrelet terrestrial habitat that must be contained within any reserve solution. Targets were based on science advice and recommendations within the literature (see Methods).

Habitat Target Total suitable habitat* 70% 50% 30%

*

Amount of habitat required (ha) 179,465.6 125,625.9 89,732.8 53,839.7

% habitat target in preexisting protected areas 8.0 11.4 15.9 26.6

Based on Mather et al. (2005).

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Table 2. Near-shore marine attributes shown to predict of the presence of foraging marbled murrelets during the pre-breeding, nesting and postbreeding periods in coastal British Columbia. Marine attributes were used to derive indices of the potential amount of marbled murrelet marine foraging habitat likely to be located within 30 km of each terrestrial planning unit (see Methods).

Marine Attribute Terrestrial habitat w/in 30 km of shoreline M1 M2 M3

Literature Source Distance (km) from terrestrial habitat to saltwater shoreline CMMRT - Canadian Marbled Murrelet Recovery Team (2003), Kuletz (2005), D. Lank, Simon Fraser University, unpublished data

M4 M5
*

Day et al. (2003), Kuletz (2005), Burger et al. (2008), Ronconi (2008) Day et al. (2003), Burger et al. (2008), Ronconi Depth (m) of marine habitat (2008) Ronconi (2008), Barrett (2008), Yen et al. * (2004), Robards et al. (1999), Ostrand et al. Distance (km) of marine habitat to nearest sandy shoreline (2005) Ronconi (2008), Barrett (2008), Yen et al. * Relative amount (m) of sandy shoreline within 2km radius of marine habitat (2004), Robards et al. (1999), Ostrand et al. (2005) Simple marine foraging habitat suitability model (m1 + m2 + m4) All of the Above Distance (m) of marine habitat from terrestrial shoreline

Sandy shoreline is defined here as in Ronconi (2008) and Barrett (2008).

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Figure 1. The south-central coast study region of British Columbia. The study region was divided into 100 hectare hexagons (grey). The distance to nearest saltwater shoreline, area of suitable terrestrial marbled murrelet nesting habitat (green) and current protected status (red) was determined for each of the 17,479 hexagon planning units.

Figure 2. Kappa statistic comparisons of the best solutions from the six target scenarios. The terrestrial value best solution is compared to each of the six considered terrestrial value+ marine value best solutions, with the two habitat values weighted equally (50% each).

Figure 3. Correlation comparisons of the summed solutions from the six target scenarios. The terrestrial value summed solution is compared to each of the six considered terrestrial value+marine value summed solutions , with the two habitat values weighted equally (50% each).

Figure 4. Correlation comparisons of the summed solutions from three of the target scenarios (30, 50 and 70 percent habitat), comparing the (100%) terrestrial value summed solution to each of ten terrestrial value+ marine value summed solutions, where the relative weight of the marine value changes incrementally starting with 10% marine value (90% terrestrial value) to 100% marine value (0% terrestrial value).

17

Figure 1.

18

Figure 2.

100 95 90 85

Kappa (%)

80 75 70 65 60 55 50 30% locked-in 50% locked-in 70% locked-in 70% 50% 30%

19

Figure 3.

1.00 0.99 0.98 0.97

Correlation (R2)

70% locked-in 70% 50% locked-in 30% locked-in 50% 30%

0.96 0.95 0.94 0.93 0.92 0.91 0.90

20

Figure 4.

1.00 0.95 0.90

Correlation (R2)

0.85 0.80 0.75 0.70 0.65 0.60 0.55 70% target 50% target 30% target

21