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Volume 10, Issue 2 e02579
Innovative Viewpoints
Open Access

Predator recovery, shifting baselines, and the adaptive management challenges they create

Kristina M. Cammen

Corresponding Author

Kristina M. Cammen

School of Marine Sciences, University of Maine, Orono, Maine, 04469 USA

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Douglas B. Rasher

Douglas B. Rasher

Bigelow Laboratory for Ocean Sciences, East Boothbay, Maine, 04544 USA

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Robert S. Steneck

Robert S. Steneck

Darling Marine Center, University of Maine, Walpole, Maine, 04573 USA

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First published: 12 February 2019
Citations: 25
Corresponding Editor: Hunter S. Lenihan.

Abstract

Recent species recoveries following historical depletion have been widely celebrated as conservation success stories. However, the recovery of highly interactive species, particularly predators, generates new management challenges that arise from their potential for wide-ranging effects on local ecosystems and their poorly understood ecology. In marine systems, many pinniped species share parallel histories of depletion, recovery, and human conflict. Recovering from post-exploitation populations of small size, these pinnipeds have returned to their present abundance from a largely absent, or severely reduced, recent role in many coastal ecosystems. To address the challenges arising today from real or perceived overabundance of protected pinniped species, we evaluate the prehistorical, historical, and contemporary abundances of six pinniped species that breed in the contiguous United States. This review highlights gaps in current knowledge that limit the implementation of ecologically grounded approaches to adaptive management of protected species in a time of shifting, or lifting, baselines. To address these gaps will require a diverse cadre of natural and social scientists as well as stakeholders to tackle the questions of how we define recovery at a species or ecosystem level, and when we have reached this point, how we move forward in a way that does not repeat a history of depletion, conservation, and recovery. Doing so will require an understanding of what role highly interactive species play in their ecosystems and how this role shifts with changes in ecological context, as well as the sociological and economic impacts of species restoration to humans. This knowledge is integral to the ongoing transition from a focus on preventing species extinction to new, and often unanticipated, challenges arising from the functional implications of species recovery.

Introduction

Throughout the past several centuries, the predominant population trend observed among higher order predators worldwide has generally been one of decline (Prugh et al. 2009, Estes et al. 2011, Ripple et al. 2014). Yet, today, notable exceptions exist in cases of successful conservation efforts leading to recovery and population growth (Norris 2004, Roman et al. 2013). Beyond well-warranted celebrations, these successful conservation efforts often yield unintended consequences, both ecological and societal (Marshall et al. 2016). For example, in many cases, recovery leads to increases in human–wildlife conflict, claims of overabundance, and public calls for changes to existing conservation policies (Roman et al. 2015, Silliman et al. 2018).

When examining the historical ecology of human interactions with wildlife across the globe, we find an oft-repeated storyline of exploitation and natural resource depletion followed by varied attempts to conserve declining populations. While some species remain stuck in a continuous decline or loop of unsuccessful or only moderately successful conservation efforts (e.g., Atlantic cod, Hutchings and Rangeley 2011; and northern right whales, Kraus et al. 2005, respectively), select species have experienced population growth, achieving or surpassing recovery targets (e.g., some fish stocks, Worm et al. 2009; bald eagles, Watts et al. 2008, Sorenson et al. 2017; wolves, Bruskotter et al. 2013). Following successful population growth, managers and policy makers must decide which path to take forward beyond recovery (Fig. 1). Do we retain the status quo under these shifting baselines by leaving conservation measures in place, accepting that this may lead to continued population growth until natural controls (top-down or bottom-up) limit carrying capacity? Or do we reconsider the path forward (i.e., adaptive management) to reduce or reverse conservation measures, risking beginning anew a cycle of depletion, conservation, and recovery? This discussion is particularly relevant to highly interactive species, who play a significant role in larger ecosystem dynamics (Soulé et al. 2003), and can at times be contentious, particularly in the case of top predators.

Details are in the caption following the image
An adaptive management perspective on the path of protected species management in response to human-induced depletion. Following depletion [step 1], when conservation efforts [step 2] lead to recovery [step 3], the potential paths diverge to include continued species protection [step 4a], reduction in protection status [step 4b], or changes in conservation policies [step 4c]. In many cases today, the path following population recovery is unclear. For example, following population recovery, pinniped species currently remain protected under the US Marine Mammal Protection Act (MMPA), but may lose supplemental protection provided by the US Endangered Species Act (ESA). In response to increased human conflict with growing pinniped populations, some stakeholders have called for more extreme policy change (e.g., population control), which if not carefully managed may restart the cycle anew.

Framed within an adaptive management cycle for protected species, here we consider the historical and contemporary knowledge available to us to inform future management of one group of highly interactive species, the pinnipeds (seals and sea lions) that have shown impressive capacity for recovery across many diverse ecological and historical contexts. Historically, almost all pinniped species have been hunted for resource use and/or population control, resulting in precipitous reductions in abundance often to the point of local extirpation (Lotze and Milewski 2004), and in a few cases extinction (McClenachan and Cooper 2008). More recently, shifts in public perception of marine mammals as charismatic megafauna have led to the implementation of local, national, and international protections. Many of these conservation measures have been successful, resulting in the rapid and recent growth of pinniped species (Magera et al. 2013), sometimes to the point of perceived (or real) overabundance. Throughout recent history, growing pinniped populations have incited concern due to perceived competition with commercial and recreational fisheries (Cronin et al. 2014, Cook et al. 2015, Hansson et al. 2018). This emotionally charged issue arguably stems from a relatively narrow ecological view of pinnipeds—primarily as predators of commercially valuable natural resources. Such conflicts are exacerbated by the fact that, like for most marine megafauna, we have limited knowledge of their ecology and the resultant ecological impacts of their recovery (Estes et al. 2016).

To address the real or perceived overabundance of protected pinniped species through policy requires a deep understanding of their historical abundance, the ecological roles these species play, as well as what has in the past and now controls their populations. Facing growing conflict and uncertainty regarding how to adaptively manage recovering pinniped populations, it seems prudent to review both the historical and contemporary ecologies of these species. Here, we do so for pinnipeds that breed in the contiguous United States, focusing on six species within this area that share a management system, exhibit parallel positive historical trajectories, and face relatively similar contemporary issues of human conflict following recovery. In doing so, we provide the historical context we feel is vital to making informed decisions about future management. We then highlight gaps in our perceptions and knowledge of pinniped ecology that limit implementation of ecologically grounded approaches to protected species management.

Focal Species

Six pinniped species currently breed in the contiguous United States: California sea lion (Zalophus californianus); Steller sea lion (Eumetopias jubatus); northern fur seal (Callorhinus ursinus); northern elephant seal (Mirounga angustirostris); harbor seal (Phoca vitulina); and gray seal (Halichoerus grypus; Table 1). These species include both phocids (true seals) and otariids (sea lions and fur seals), with characteristic differences in several aspects of their ecology. Otariids and elephant seals tend to be larger with more pronounced sexual size dimorphism. They breed primarily on land in large breeding colonies where males defend territories and mate with multiple females (Boness et al. 2002). Gray and harbor seals are smaller, less gregarious, and do not utilize a land-based territory defense mating strategy (Boness et al. 2002). All six pinniped species feed primarily on fish with some overlap in prey (Bowen et al. 1993, Bowen and Harrison 1996, Winship and Trites 2003), though otariids are generally able to forage on prey of larger size (e.g., adult pollock and salmon). In waters surrounding the contiguous United States, only phocids inhabit the North Atlantic, an environment generally characterized by lower species and functional diversity compared to the North Pacific (Estes et al. 2013), where both otariids and phocids are present. In the face of these differences, and several others, we contend the shared historical trajectories of depletion and recovery of these six pinniped species across ocean basins warrants review and consideration.

Table 1. Current estimates of pinniped population size and recent trends in population growth in the contiguous United States
Species Stock Population size Recent population trends
California sea lion, Zalophus californianus United States 296,750 (2008)a +5.4%/yr (1975–2008), excluding El Niño years
Steller sea lion, Eumetopias jubatus Eastern (southeast Alaska to California) 60,131–74,448 (2009–2013)b +4.18%/yr (1979–2010)
Northern fur seal, Callorhinus ursinus California 12,844 (2011)a +24%/yr (1972–1982), including immigration
Northern elephant seal, Mirounga angustirostris California 179,000 (2010)c +3.8%/yr (1988–2010)
Harbor seal, Phoca vitulina richardii California 30,968 (2012)a +3.5%/yr (1982–1995) d
Harbor seal, P. vitulina richardii Oregon/Washington Coast 24,732 (1999)a +7%/yr (1983–1992); +4%/yr (1983–1996)
Harbor seal, P. vitulina richardii Washington Inland Waters 13,692 (1999)a +6%/yr (1983–1996); currently stable
Harbor seal, P. vitulina vitulina Western North Atlantic 75,834 (2012, Maine)e +6.4%/yr (1981–2001)f
Gray seal, Halichoerus grypus atlantica Western North Atlantic Unknown (United States); 331,000 (2012, Canada)e United States: increasing; Canada: +12.8%/yr (1970s–1997); +4%/yr (2007–2010); +2.8%/yr (2010–2012)
  • a Carretta et al. (2015).
  • b Allen and Angliss (2015).
  • c Lowry et al. (2014).
  • d Lowry et al. (2008).
  • e Hayes et al. (2018).
  • f Waring et al. (2010).

Historical ecology—an era of exploitation

Historical ecology, broadly defined, is the study of past interactions between humans and natural ecosystems, with the goal of improving our understanding of the present (Jackson et al. 2001, Szabó 2015). Interdisciplinary by nature, historical data are drawn from both archival sources and the natural sciences, but are rarely, if ever, comprehensive. Here, we draw upon archaeological records, historical accounts, and government documents to briefly review the long history of human interaction with pinniped populations in the United States, providing a baseline of sorts with which to evaluate the current abundance and distribution of pinnipeds. The historical records provide insights into baselines of relative abundance, from which we can derive the relative role of pinnipeds in local ecosystems, accepting the limitations associated with assuming a direct relationship between abundance and ecological impact. Furthermore, these records clearly illustrate a history of depletion, step 1 of the adaptive management cycle depicted in Fig. 1.

Aboriginal subsistence

Archaeological records suggest that human hunting for marine mammals began as early as 8500–12,000 yr ago in the contiguous United States (Braje et al. 2011). Where present, otariids are generally more common than phocids in the faunal record (Fig. 2a), but rather than (or in addition to) reflecting differences in abundance, this variation likely reflects hunter bias. Native Americans are thought to have targeted smaller phocids, which were likely less desirable and/or more difficult to catch, only after overexploitation of the preferred larger pinnipeds (Hildebrandt and Jones 1992, Jones and Hildebrandt 1995, Porcasi et al. 2000). In the northeast United States, where there are no native otariids, the archaeological remains of gray and harbor seals are found in approximately equal ratios (Fig. 2b). Some authors have suggested that the relatively low abundance of seal remains in comparison with other fauna, in particular cod, may reflect relatively low early (~4000 BP) prehistoric pinniped abundance in the Northwest Atlantic (Bourque et al. 2008). If true, this represents a drastic shift from the contemporary view of seals as predators of cod to considering large cod (averaging over 1 m in length from archaeological deposits aged 500–4500 BP; Jackson et al. 2001) as competitors of seals (via shared predation on small prey fish). Following an apparent decline in cod, historical records suggest that seals in the western North Atlantic were abundant and hunted by Native Americans by the time of European contact in the late 1500s (de Champlain 1922).

Details are in the caption following the image
Relative abundance of specimens from pinniped species recovered at well-studied archaeological sites on the (a) west coast and (b) northeast coast of the United States. Numbers within pie charts represent the total number of pinniped specimens identified at each site. Values are raw counts of bones (i.e., number of individual specimens rather than minimum number of individuals). Data were compiled from the following sources: (a) Etnier (2007), (b) Colten (2002), (c) Lyman (1989), (d) Hildebrandt (1984), (e) Hildebrandt and Jones (1992), (f) Braje and DeLong (2009), (g) Rick (2007), (h) Walker et al. (2002), (i) Ingraham et al. (2015), and (j) Spiess and Lewis (2001).

A relative surplus of presently rare species in the archaeological record on the west coast of the United States suggests a shift in the dominant species along this coastline. For example, the remains of Guadalupe fur seals (Arctocephalus townsendi) are common in archaeological sites in southern California (Rick et al. 2009), though this species was extirpated in the United States in the late 1800s. In addition, an abundance of northern fur seal remains suggests that this species may once have been a year-round resident that bred on the mainland (Burton et al. 2001, Newsome et al. 2007), though today this species breeds only in small numbers on offshore islands in California. In contrast to the relative surplus of fur seals in the archaeological records, northern elephant seals are notably, and surprisingly, scarce relative to their contemporary abundance (Rick et al. 2011). It has been suggested that elephant seals were displaced early on from coastal sites to remote island settings by terrestrial predators (e.g., grizzly bears and mountain lions) and Native American settlements (Rick et al. 2011), with records of these early hunts lost to rising sea levels (Braje et al. 2011).

Commercial hunts

Following European contact, pinniped species in the United States became the target of extensive commercial hunts during much of the 1800s (Scammon 1874). Targeted for their blubber, fur, hides, and trimmings (testicles, whiskers, and gall bladders), these hunts led to precipitous reductions in pinniped abundance and local extirpation of several species, including northern and Guadalupe fur seals (Starks 1922) and northern elephant seals (Townsend 1885). California and Steller sea lions became the focus of subsequent hunts, but the loss of markets and early, localized efforts to protect sea lion rookeries prevented their regional extirpation (Bonnot 1928). On the east coast of the United States, hunts focused primarily on gray seals, the larger and more accessible of the phocids, which were hunted until commercial extinction in the mid-seventeenth century (Mowat 1984). Harbor seals were a relatively minor component of the commercial hunts on either coast, likely because they were smaller, less abundant, and more difficult to catch (Rowley 1929, Mowat 1984).

Bounty programs

Cessation of commercial hunts did not end the harvest of pinniped species in the United States. Rather, some species, particularly harbor seals, were more dramatically impacted by subsequent bounty programs, initiated in response to the perception of pinnipeds as significant predators of commercially important fish species. Bounties in Maine (Lelli and Harris 2006), Massachusetts (Lelli et al. 2009), Oregon (Pearson and Verts 1970), and Washington (Newby 1973), from the late 1800s until as recently as 1972, are estimated to have lethally removed over 100,000 seals and sea lions (Table 2). Harbor seals were the primary targets of these bounty programs, which led to severe depletion of their populations on both east and west coasts. These programs resulted in the extirpation of harbor seal breeding colonies south of Maine (Katona et al. 1993) and highly reduced populations in Oregon and Washington (Pearson and Verts 1970). Already reduced populations of gray seals in the northeast United States were also susceptible to targeted bounties, which ultimately resulted in their complete or near complete extirpation in United States waters. Steller and California sea lions were impacted to a lesser extent, and northern elephant seals and fur seals were not targeted due to their low abundance and the early implementation of laws to protect these species.

Table 2. State-financed bounty programs for pinnipeds in the contiguous United States, with species listed in decreasing order of the number of individuals killed
State Years Species Estimated no. of pinnipeds killed
Mainea, b 1891–1905, 1937–1945 Harbor seals, gray seals 72,000 to 135,000 seals
Massachusettsb 1888–1908, 1919–1962 Harbor seals, gray seals 72,000 to 135,000 seals
Washingtonc 1915–1960 Harbor seals, Steller sea lions, California sea lions 1943–1960: 17,000 harbor seals, 900 sea lions
Oregond 1919–1933 (statewide), 1935–1972 (Columbia River) Harbor seals, Steller sea lions, California sea lions 1925–1933: 3300 harbor seals, 3900 sea lions; 1935–1972: 3150 seals and sea lionse
  • a Lelli and Harris (2006).
  • b Lelli et al. (2009).
  • c Newby (1973).
  • d Mate (1980).
  • e A state seal hunter also killed 500–1000 pinnipeds in the Columbia River, 1959–1970.

Over this period of exploitation, it is clear that the abundance, and presumably ecological role, of pinnipeds in coastal and island ecosystems significantly diminished, in a targeted and non-random order. As demonstrated elsewhere (e.g., fishing down the food web; Pauly et al. 1998), humans tended to remove the largest pinnipeds from the ecosystem first, followed by the smaller species. The ecological impacts of pinniped removal on local ecosystems are unclear and muddled by the synchronous removal of large biomass from lower trophic levels through targeted fisheries; however, theory and empirical studies suggest generally that the loss of upper trophic-level predators from a system can undermine ecosystem resilience and disrupt valuable ecosystem services (Dobson et al. 2006, Estes et al. 2011, Ripple et al. 2014). For example, in contrast, or in addition to, their perceived dominance as coastal predators in contemporary ecosystems, pinnipeds, particularly on the west coast, may have been historically important prey species that more directly linked marine and terrestrial systems.

Contemporary ecology—an era of recovery

Given the well-described impacts of predator removal (Dobson et al. 2006, Estes et al. 2011, Ripple et al. 2014), it seems reasonable to assume that the recovery of marine predators would also have wide-ranging effects on coastal and ocean ecosystems. Highly interactive species, including large marine predators, play an important role in shaping contemporary ecosystems (Estes et al. 2016). Yet, our poor understanding of the mechanisms underlying changes following predator loss makes it difficult to predict ecosystem-level impacts of predator recovery (Estes et al. 2011), particularly when we acknowledge that recovery does not necessarily follow the same path as decline (Hughes et al. 2005), and our coastal ecosystems have changed dramatically across trophic levels from pre-exploitation baselines (Jackson et al. 2001). Here, we review recent population assessments to evaluate the recovery trajectories of all pinniped populations in the contiguous United States and consider shared paths, processes, and outcomes across diverse species and ecological contexts. The past few decades for pinnipeds in the United States are a clear demonstration of steps 2 and 3, protection and recovery, of the adaptive management cycle depicted in Fig. 1.

Protection and recovery

The long history of pinniped exploitation came to an end in the United States when the Marine Mammal Protection Act (MMPA) was passed in 1972. This Act superseded several prior pinniped protection laws that had been enacted on local and state scales, allowing for early recovery in some species. In addition, since its passing further protections have been awarded to some marine mammals, including the Steller sea lion under the jurisdiction of the United States Endangered Species Act (ESA). These federal protections have been largely successful, resulting in population growth of all six pinniped species that breed within the contiguous United States (Fig. 3). While there are nuanced differences among the recovery trajectories of these six species (further details provided in Appendix S1), the general trend of recovery is shared among phocids and otariids across the Northwest Atlantic and Northeast Pacific alike (with limited exceptions in Alaska; National Research Council 2003), despite differences in community dynamics and historical contingencies that ecological theory suggests should dictate recovery trajectories (Stier et al. 2016). Rather, these cases suggest that pinniped species share an impressive ability to recover despite their relatively slow life histories and that recovery trajectories are driven largely by management efforts.

Details are in the caption following the image
Trends in population estimates for pinnipeds in the contiguous United States. Data depicted are estimates of pup production of California sea lions (Carretta et al. 2015) and northern elephant seals (Lowry et al. 2014) from California; pup production of northern fur seals on San Miguel Island, California (Carretta et al. 2015); counts of non-pup Steller sea lions throughout the range of the eastern distinct population segment (Allen and Angliss 2015); counts of all harbor seals at haulouts during the molting or pupping seasons in California (Carretta et al. 2015), Washington (Jeffries et al. 2003), Oregon (Brown et al. 2005), and Maine (Waring et al. 2010, Hayes et al. 2018); and pup production of gray seals on Muskeget Island, Massachusetts—the largest gray seal colony in the United States (Wood LaFond 2009). Estimates are presented as a proportion of maximum count in the last five decades. Vertical line depicts enactment of the US Marine Mammal Protection Act in 1972. A more detailed review of the individual recovery trajectories for each of our focal species is presented in Appendix S1.

Similar to other cases of marine species recovery (Lotze et al. 2011), pinniped recovery was driven primarily by the reduction in human hunting, reflecting a shift in cultural values toward appreciative non-consumptive use of marine mammals. In several cases, where local breeding colonies had been extirpated, immigration also played an important role in facilitating recovery (e.g., northern elephant seals from Mexico, Stewart et al. 1994; northern fur seals from the Bering Sea, Peterson et al. 1968; and gray seals from Canada, Wood et al. 2011). In contrast to the recovery of terrestrial predators, habitat fragmentation and the need for corridors (Rouget et al. 2006) do not pose the same hindrance to pinniped recovery in coastal ecosystems. Rather, immigration has led to population growth at rates faster than would have been expected based on pinniped's relatively low reproductive capacity. The recovery of these species does not appear visibly impaired by reductions in genetic diversity from pre-exploitation populations, as indicated for the endangered Hawaiian monk seal (Schultz et al. 2009), or drastic reductions in commercially exploited fish stocks that serve as the primary prey base for some of these species, as suggested for the endangered Steller sea lion population in Alaska (Trites and Donnelly 2003). The latter, while somewhat surprising, may be explained by a generalist diet exhibited by most pinniped species. We also cannot discount the positive additional impacts from the recovery of river-migrating forage fish in the Gulf of Maine (Day 2006) and salmon in the northwest United States (Williams et al. 2006), which has occurred with or shortly following initial pinniped population growth and could have contributed to pinniped recovery in both ecosystems (Samhouri et al. 2017).

Altered community dynamics may have more significantly impacted recent population trends among these pinniped species. There are today several cases where recovery has been slow or reversed in recent years, and competition with other pinnipeds, a reduced forage base, or predator-induced mortality is often cited as a potential explanation. For example, in California, a second decline (following initial recovery) of Steller sea lions (Stewart et al. 1993, Pitcher et al. 2007) has been attributed to population growth of California sea lions (Bartholomew 1967). California sea lion populations may in turn be controlled by competition with northern fur seals (DeLong and Melin 2002), and their pups are now experiencing food limitation, apparently because of declines in forage stocks (McClatchie et al. 2016). At several sites in the northeast United States, as well as several other locations across the North Atlantic, harbor seal populations have declined when sympatric gray seal populations have recovered (Waring et al. 2010), possibly as a result of competition for prey or haulout space and/or differential disease susceptibility. At Sable Island in Nova Scotia, Canada, the decline of a once dominant harbor seal population has been attributed in part to increased shark predation (Lucas and Stobo 2000) and decreased prey availability, both factors that are likely exacerbated by growing gray seal populations (Bowen et al. 2003). Gray seals are also increasingly recognized as reservoir species that can transmit diseases across species and geographies (Puryear et al. 2016), potentially exacerbated by climatic change (Lavigne and Schmitz 1990, Burek et al. 2008). Diseases such as avian influenza and phocine distemper virus, which may circulate enzootically in gray seals (and likely Arctic pinnipeds that wander into United States waters; Duignan et al. 1997, Hall et al. 2006), have caused several large-scale mortality events of harbor seals on both sides of the North Atlantic (Härkönen et al. 2006, Anthony et al. 2012, Bodewes et al. 2015). As has been empirically and theoretically suggested across diverse ecosystems (Stier et al. 2016, Samhouri et al. 2017), in the case of California and Steller sea lions, as well as gray and harbor seals, the order of recovery of both potential prey and competitors may be influential in shaping contemporary ecosystems and determining persistence of these highly interactive species.

Consequences of recovery

Currently, much of the conversation regarding pinniped recovery in scientific, management, and public spheres remains singularly focused on pinnipeds as predators. As top, or near-top, predators in coastal ecosystems, pinnipeds have and continue to be viewed as a threat to commercial and recreational fisheries (MacKenzie et al. 2011, Houle et al. 2016). Yet their influence on fish stocks relative to direct human removal of fishes has received little attention (Darimont et al. 2015). The role of pinnipeds as prey has also drawn increasingly negative attention in the public sphere, as they are blamed for attracting sharks to swimmable waters. In the northeast United States, increases in historically depleted shark populations have recently been documented following local pinniped recovery (Skomal et al. 2012), but the results of more recent population assessments of sharks and seals are still pending. It seems possible that the perceived current overabundance of pinnipeds may be an outcome of mesopredator release (Frid et al. 2008), which if true has implications for natural controls of pinniped populations as their predators recover.

As pinniped populations recover, their potential impact on habitats, and water quality in particular, at dense breeding colonies and haulout sites, has received increased attention. While marine mammals are known to release nutrients in ocean ecosystems through their excrement, carcasses, and other bodily fluids (Roman and McCarthy 2010, Moss 2017), their potential contribution to productivity remains relatively poorly understood, particularly for pinnipeds. While past research suggests that pinniped excreta can enrich local algal communities (Hansen 1972), preliminary research on gray seals in the northeast United States refutes public concerns that seal colonies contaminate local waters (public communications Woods Hole Oceanographic Institution, Study Looks at Gray Seal Impact on Beach Water Quality, December 18, 2012, https://www.whoi.edu/news-release/Gray-Seals-Water_Quality).

To more broadly understand the ecological consequences of pinniped recovery requires studies that consider these highly interactive species beyond any single role in the ecosystem. Yet, few studies consider pinnipeds from a whole-ecosystem perspective, with limited exceptions from the Benguela and California Current ecosystems (Cochrane et al. 2004, Melin et al. 2012). While difficult to envision and complete, these are the types of studies that will be most valuable to efforts toward adaptive, ecosystem-based management. We require studies that explicitly and holistically consider how the role of pinnipeds has changed as populations shift in size or distribution, if we are to effectively incorporate ecology into protected species management.

Recovery ecology

The current management system for marine mammals in the United States aims to maintain marine mammals as functioning elements of their ecosystems (Marine Mammal Protection Act of 1972, 16 USC § 1361 [1972]). We, and others, contend that to effectively implement such ecologically grounded approaches to protected species policy requires both an appreciation for the historical context that shapes contemporary ecology and a broad understanding of the ecological complexity of a system (Matthiopoulos et al. 2008). If we, as scientists, managers, or the general public, ignore this complexity in shaping our conservation policies moving forward beyond recovery, we risk beginning anew a cycle of depletion–conservation–recovery (Fig. 1). The uncertainty that we currently face regarding how to move beyond recovery for protected species is arguably in large part due to current gaps in our understanding of the ecology of species recovery, particularly of upper trophic-level predators. These issues, of course, are not unique to pinnipeds, but apply across many other managed terrestrial and marine predators (Marshall et al. 2016).

The processes, outcomes, and implications of species recovery are increasingly well understood in certain domains of ecology. For example, the rapidly growing field of restoration ecology, which has traditionally focused on sessile foundational species, has provided insights into how best to re-establish foundational species in degraded habitats (Zedler 2000) and how to evaluate the benefits of resulting ecosystem services (Bullock et al. 2011). Similarly, studies of community recovery and resilience, for example in corals, have elucidated the importance of species composition and demographic processes (e.g., recruitment) in determining recovery success (Lenihan et al. 2011, Kayal et al. 2018). Yet, gaps remain related to the recovery of highly interactive species at upper trophic levels. These species have the potential to exert strong impacts on the ecosystem, but in ways that are often more socially complex than foundational species, where multiple stakeholder groups may have well-aligned interest in either recovery or population control. Current gaps in our understanding largely revolve around how to quantitatively assess the ecological impacts of changing species abundance and evaluate these impacts within the context of complex social–ecological systems. Given that species depletion, not recovery, was the norm until only recently, it is not surprising that we lack understanding in these areas.

To expand restoration ecology and studies of community recovery to consider upper trophic-level species and the associated human social issues that arise with such efforts will require a diverse cadre of natural and social scientists, as well as associated stakeholder groups. Together, these scientists and stakeholders must tackle the questions of how we define recovery at a species or ecosystem level, and when we have reached this point, how we move forward in a way that does not repeat a history of depletion, conservation, and recovery (Fig. 1). Doing so will require an understanding of what role highly interactive species play in their ecosystems and how this role shifts with changes in ecological context. It will require consideration of the sociological and economic impacts of species restoration to humans and a shift in perception of lifting baselines for recovering species (Roman et al. 2015). The management challenge posed here is not one that should be approached as though it can be easily fixed, but rather it should be explored and revisited regularly to find the best path forward through ecologically and socially conscious adaptive management.

Interdisciplinary, collaborative, and multi-stakeholder groups such as the Northwest Atlantic Seal Research Consortium have begun to tackle these challenges for gray and harbor seals in one region of our study. Their approach to dealing with perceived and real conflict with growing pinniped populations has been to engage fishermen and community members directly in science and conservation efforts. In the northwest United States, multi-stakeholder coalitions, including the fishing industry, environmental organizations, and tribal community members, have also worked with state and federal managers to tackle issues at a local scale in an attempt to reduce human–wildlife conflict. Most recently, earlier this year the United States House of Representatives passed a bill entitled “Endangered salmon and fisheries predation prevention act (HR 2083)” that authorizes the issuance of permits to kill California and Steller sea lions in the Columbia River to protect salmon and other fish. This bill, which represents a new attempt to balance the diverse needs and desires of humans in the region, follows earlier efforts, codified in 1994, to amend the MMPA to include a mechanism to authorize the lethal removal of nuisance pinnipeds (Young et al. 2000). These approaches in response to an ecological process that is cause for concern prescribe a narrow solution that is specific to the localized situation and does not threaten to result in significant population decline. Within a narrow context like this, we are perhaps better equipped to understand the historical, social, and ecological complexities at play.

With approaches that integrate lessons learned from historical and contemporary ecology as well as the expertise of diverse disciplines, we are hopeful that broader ecosystem-based science and policies will evolve to better measure and adaptively manage ecological processes for abundant and highly interactive species (Soulé et al. 2003). Finding such new paths forward that include baselines that have shifted upward is integral to the ongoing transition of conservation biology from a field focused solely on preventing downward shifting baselines that trend toward species extinction to a field faced with new, and often unanticipated, challenges arising from the functional implications of protected species recovery.

Acknowledgments

We thank J. Estes, M. Hunter, B. Robinson, G. Waring, the University of Maine Ecology and Evolution of Everything seminar group, H. Lenihan, and two anonymous reviewers for their thoughtful comments and discussion that helped shape this manuscript. J. Stoll assisted with figure graphical design. K. Cammen was supported by a National Science Foundation Postdoctoral Research Fellowship in Biology under Grant No. 1523568.