Predator-prey relationships shape the population dynamics of exploited taxa (Essington and Munch, 2014). In many cases, predatory removals match or even exceed those from fishing, and thus significantly impact the maximum sustainable yield of a stock (Tyrrell et al., 2011). In tandem with empirical and theoretical advances in our understanding of predator physiology and predator-prey interactions, there has been a growing appreciation of the need to characterize population dynamics and manage fisheries in an ecological context (Yodzis, 1994; Fulton et al., 2003; Tyrrell et al., 2011; Steele et al., 2013; Stehlik et al., 2021). Small shark and ray species often take the role of mesopredator in oceanic ecosystems, consuming small fish or invertebrates while being predated upon by larger sharks, fish, and marine mammals. Due to this position, the trophic ecology of mesopredatory sharks and rays is frequently of interest to researchers and fisheries stakeholders, given their potential roles in trophic cascades and similar phenomena (Myers et al., 2007).

The spiny dogfish (Squalus acanthias) is a small mesopredatory shark commonly found in temperate waters of the Atlantic and South Pacific oceans (Veríssimo et al., 2010). It is the most abundant shark in the Northwest Atlantic, a highly productive and diverse marine ecosystem (Link et al., 2008; Dell’Apa et al., 2018). Spiny dogfish range from Canada to Florida and support an active fishery along the U.S. east coast (Dell’Apa et al., 2017). Targeted fishing of spiny dogfish in the Northwest Atlantic began in the 1980s, following the collapse of several groundfish fisheries in the region. This resulted in substantially reduced female biomass from the early-mid 1990s through the mid-2000s (Rago et al., 1998; Rago and Sosebee, 2010). The fishery primarily targets mature females (>95%) due to sexual and ontogenetic segregation. Mature females are found inshore relative to male or immature individuals, and females grow larger than males, so mature females are both more accessible and economically desirable (Rago et al., 1998; Haugen et al., 2017). This spatial segregation may result from females seeking relatively warmer temperatures for growth and pup development (Dell’Apa et al., 2014). Alternatively, a male avoidance hypothesis has been suggested, with females avoiding areas with many males due to the energetic loss of engaging in (or rebuffing) copulation, or a combination of the two (Economakis and Lobel, 1998; Sims, 2006; Dell’Apa et al., 2014, 2015).

Spiny dogfish co-occur with several ecologically and economically important teleost species, raising concern about their impact on prey and competitors in the Northwest Atlantic ecosystem, particularly as this system recovers from historical overfishing (Rago and Sosebee, 2010; Bangley and Rulifson, 2014). Once reproductive maturity is reached, spiny dogfish occupy upper trophic levels in this system and share a guild with several large bony fishes. Since the collapse of groundfish populations in the 1990s, spiny dogfish are among the most common piscivores in the Georges Bank fish community (Garrison and Link, 2000; Link and Garrison, 2002). This species preys on pelagic fishes and cephalopods in the region, including Atlantic herring (Clupea harengus), longfin inshore squid (Doryteuthis pealeii), bay anchovy (Anchoa mitchilli), Atlantic mackerel (Scomber scombrus), and Atlantic menhaden (Brevoortia tyrannus) (Overholtz et al., 2000; Overholtz and Link, 2007; Moustahfid et al., 2009a, 2009b; Bangley and Rulifson, 2014). Mature females overwintering off North Carolina primarily feed on teleosts, which also form a large part of the diets of striped bass (Morone saxatilis), bluefish (Pomatomus saltatrix), and spotted seatrout (Cynoscion nebulosus) along the U.S. east coast (Hartman and Brandt, 1995; Overton et al., 2008; Bangley and Rulifson, 2014). Fishery stakeholders have expressed concern that spiny dogfish are hampering recovery of collapsed fish stocks, whether through predation or competition, though this hypothesis lacks empirical support (Fogarty and Murawski, 1998; Link and Garrison, 2002; Myers et al., 2007; Pitchford et al., 2020). Conversely, historical fishing pressure has shaped the population dynamics of spiny dogfish, which very likely has an impact on overall consumptive removals by spiny dogfish (Rago et al., 1998; Rago and Sosebee, 2010). Accordingly, further research is needed to assess the impact of this predator on prey, competitors, and regional fisheries (Bangley and Rulifson, 2014).

Adopting ecosystem-approaches to fisheries management (EAFM) necessitates a well-developed understanding of the underlying mechanisms and interactions between a managed species and the environment, including predator-prey dynamics (Link and Marshak, 2021). Due to sexual and ontogenetic segregation, known ontogenetic shifts in diet, and seasonal migration patterns, spiny dogfish likely assume various predatory roles throughout their life cycle (Koen Alonso et al., 2002). In this context and to support EAFM efforts, the goal of this study is to quantify consumptive removals of key prey species by spiny dogfish in the Northwest Atlantic, considering factors such as sex, maturity stage, and season. We also sought to assess linkages between seasonal consumption estimates and several environmental and biotic covariates.

This study is the first to quantify spiny dogfish prey consumption by sex and maturity stage. Our model-based spatial distributions of these predator groups generally confirmed previous findings showing sexual segregation, with mature females concentrated inshore and males (both stages) and immature females located farther offshore, though all four predator groups were found across the entire study area (Dell’Apa et al., 2014; Haugen et al., 2017). The four species evaluated in this study (spiny dogfish, Atlantic menhaden, Atlantic herring, longfin inshore squid) showed strong seasonal shifts in distribution, and spatial patterns in consumption by spiny dogfish generally followed prey distributions (Hatfield and Cadrin, 2002; Kanwit and Libby, 2008; Carlson et al., 2014; Buchheister et al., 2017). For multiple predator-prey group combinations, the prey of interest was absent from predator stomachs for multiple years. This was likely due to small sample sizes, and consumption estimates for those years were set to zero because each year of the study period was modeled independently. While it is improbable that no interactions occurred between those prey and predators in these years, consumption was likely low such that our results likely provide useful information on the temporal patterns of consumption of key prey. Modeling the year covariate as a random walk or with a first order autoregressive structure to “borrow” information across years has been used previously in VAST to address low sample size issues, and implementing such an approach with data on predator-prey interactions represents a potentially fruitful area of future research (Thorson, 2019).

Of the three annualized covariates representing broad-scale climatic influences on the Northwest Atlantic ecosystem, the AMO was the most consistently linked with consumption of key prey by spiny dogfish. Positive linkages were found between consumption and the AMO for immature females, mature males, and mature females and all three key prey species during both spring and fall. Consumption of longfin inshore squid was positively correlated with AMO consistently for immature females and mature males, while the consumption of other prey in spring by immature males was negatively correlated with this index. Longfin inshore squid populations are known to fluctuate in response to environmental conditions and have been found to correlate with AMO (Collie et al., 2008; Nye et al., 2014; van der Kooij et al., 2016), which may explain their increased consumption by immature female and mature male spiny dogfish during positive AMO phases. Unlike other predator groups, mature female spiny dogfish are typically found in nearshore environments, which may explain why their consumption was less frequently tied with AMO (Haugen et al., 2017). However, both the AMO and gastric evacuation rate approach used to calculate consumption are closely linked to temperature, which raises the possibility that the statistical significance detected was confounded by temperature effects.

The GSI and the NAO were less correlated with annual consumption indices relative to the AMO, though both GSI and NAO were positively linked with consumption of Atlantic menhaden and Atlantic herring by mature females during fall. GSI and NAO are known to be correlated, so the similarities in their linkages with trends in annual consumption are not unreasonable (Taylor and Stephens, 1998; Bellucci and Richards, 2006). However, as the climate indices chosen here did not have a consistent temporal scale, we did not attempt to attribute between-index differences to a specific cause. While the exact mechanisms for the linkages between consumption and these climate indices are unknown, it may be that the position of the Gulf Stream alters habitat suitability for mature females and their prey (and therefore predator-prey interactions) in fall due to shifting temperature regimes (Hurrell and Deser, 2010). Linkages between the consumption of Atlantic herring, longfin inshore squid, and aggregate other prey by immature males, immature females, and mature males during spring may also be tied to shifting temperature patterns or indirect effects on productivity (Feng et al., 2014).

Harvest of prey was found to have both positive and negative correlations with spiny dogfish consumption. Positive correlations, such as with the consumption of Atlantic herring by multiple predator groups during spring and fall, may reflect bottom-up controls on consumption due to prey availability. Both consumption and harvest of prey can increase as prey availability increases (Beverton and Holt, 1993; Smith and Smith, 2020). In contrast, negative correlations between consumption and harvest, as documented for the consumption of Atlantic menhaden in the fall and longfin inshore squid in both seasons by mature females, could be driven by competition between spiny dogfish and fishing fleets for available prey (Hjermann et al., 2004). In this case, it would be challenging to determine whether fishing pressure limits predation or vice versa. Alternatively, it is possible that spiny dogfish are more effective predators of certain prey in habitats that differ from those where harvesting operations are most effective. Commercial fishing tactics and mobile piscivorous predators have distinct constraints, which may not always align (Alós et al., 2012; Olsen et al., 2012). This could create a scenario where prey distribution may favor spiny dogfish predation in one year and commercial harvest in another, creating the appearance of competition.

Significant linkages between the two remaining proxies for prey availability, modeled seasonal prey biomass density and seasonal predator-prey overlap, and consumption represented three general categories. The first category included those that support the hypothesis that prey availability governs consumption. Positive correlations between prey availability and consumption were detected for several predator-prey group combinations but were most prevalent for the consumption of Atlantic herring during both seasons and Atlantic menhaden in the fall. While no significant linkages were found between longfin squid abundance and consumption, there were significant correlations between overlap of immature female and mature male spiny dogfish and longfin inshore squid in fall, suggesting the importance of local prey availability due to predator-prey co-occurrence as opposed to broader, ecosystem-level availability resulting from shifts in prey population size (Schmitz et al., 2017).

The second category of linkages represented negative correlations between availability of one prey and consumption of another by spiny dogfish. These inverse relationships were detected between Atlantic herring and Atlantic menhaden, and may reflect “prey switching” (Murdoch, 1969). Prey switching occurs when predators preferentially consume the most available prey species, and is derived from optimal foraging theory, which predicts that there are circumstances where it is favorable for a predator to choose a more beneficial source of prey even if it means missing opportunities to hunt other prey species (Hubbard et al., 1982). Prey switching has been documented previously in the Northwest Atlantic (Fogarty et al., 1991; Overholtz et al., 2000; Link and Garrison, 2002; Buren et al., 2012), though this study is the first to show potential prey switching between Atlantic herring and Atlantic menhaden by spiny dogfish. While not explicitly modeled, prey switching is a key part of the theoretical underpinning for Holling’s Type III functional response relationship, which has been reported to best describe predation by most piscivores in the Northwest Atlantic, including spiny dogfish (Holling, 1959; Smith and Smith, 2020).

The third category of significant linkages included positive relationships between the availability of one prey species and the consumption of another. This relationship was most frequently detected between the consumption of longfin inshore squid and availability of Atlantic herring in the fall. There are a few potential explanations that might support this relationship. First, adult Atlantic herring and juvenile longfin inshore squid have overlapping diets, both consuming large amounts of euphausiids and chaetognaths (Bowman et al., 2000; Jacobson, 2005). This may tie the availability of both prey species to similar covariates such that when environmental conditions favor euphausiids or chaetognaths, both Atlantic herring and longfin inshore squid populations may respond positively, either regionally or locally. Second, adult longfin inshore squid feed heavily on small fishes in the fall, including clupeids such as Atlantic herring (Jacobson, 2005). Consequently, years with greater regional herring populations may concentrate longfin inshore squid and spiny dogfish into the same foraging habitat, with greater consumption of longfin inshore squid by spiny dogfish due to their increased availability.

Sex and maturity stage both played a role in consumption of key prey by spiny dogfish. Most notably, male spiny dogfish of both maturity stages consumed negligible amounts of Atlantic menhaden, even when found in nearshore waters, except for during 2016. In contrast, both immature and mature females consumed relatively large quantities of Atlantic menhaden in nearshore waters, with Atlantic menhaden comprising the largest component of consumption by mature females in the nearshore NEAMAP survey, even exceeding unidentified fishes. The reduced consumption of Atlantic menhaden by male spiny dogfish may be due to their smaller size, or greater depth preferences, as Atlantic menhaden schools are typically found in shallower habitats close to the surface. Further, when mature male spiny dogfish move to inshore habitats, they may be pursuing females rather than foraging. In numerous cases, prey consumption by one or more predator groups had a significant linkage with a given environmental covariate or prey availability index while consumption of the same prey by one or more other predator groups did not. This supports the hypothesis that sex and maturity influence the role of spiny dogfish as a predator. Dietary changes with maturity are expected, as spiny dogfish are known to undergo an ontogenetic shift towards piscivory (Koen Alonso et al., 2002; Bangley and Rulifson, 2014). Despite this, relationships between the consumption of a prey species and covariate changed directions across predator groups only occasionally, such as in the relationship between longfin squid harvest and fall squid consumption by immature males versus mature males and females. However, this phenomenon did manifest several times for the aggregate prey category, potentially pointing to greater differences in predatory habits with prey outside the three key species considered in this study. Potential candidate prey types for future evaluation include ctenophores, mackerels, or hakes. Unidentified prey (whether unidentified invertebrate, unidentified bony fish, or simply “animal remains”) was frequently the largest component of each spiny dogfish category by mass, highlighting the information loss that occurs when prey items cannot be identified. This reinforces the importance of pursuing identification to the lowest taxonomic level whenever possible, whether through more in-depth visual examination, molecular means, or a combination of both.

One additional influence we did not examine quantitatively was the direct impact of fishing pressure on consumptive removals by spiny dogfish. As a response to the decline of groundfish stocks, directed fishing pressure on spiny dogfish increased in the 1980s. After a period of intense fishing, the estimated biomass of spawning stock females was markedly low from the mid-1990s through the mid-2000s (Rago et al., 1998). As estimated predator biomass was used to calculate consumption, this reduction in predator biomass undoubtedly had an influence on consumptive removals in the region. This may explain some of the temporal patterns seen in the consumption of Atlantic menhaden and aggregate other prey by mature females. This pattern was not consistent across all predator groups or prey species but may warrant further examination by future researchers interested in the role of fishing pressure on consumptive removals by spiny dogfish and other exploited predatory species.

Overall, prey availability was found to be an important covariate for consumption of Atlantic menhaden, Atlantic herring, and longfin inshore squid by spiny dogfish, a dominant mid to upper trophic level predator in the Northwest Atlantic. Of the consumption linkages detected, the most relevant to regional fisheries management were likely the negative relationships between Atlantic herring availability and Atlantic menhaden consumption by female spiny dogfish, and the positive linkages between Atlantic herring availability and longfin inshore squid consumption. Atlantic menhaden are currently managed using an ecosystem approach to fisheries management (EAFM). While the associated ecosystem model considered five focal species that included four Atlantic menhaden predators (Atlantic striped bass, bluefish, spiny dogfish, weakfish) and Atlantic herring as an alternative prey, the final model selected only included striped bass, as it was the most sensitive predator to changes in levels of Atlantic menhaden biomass (Chagaris et al., 2020). It has been noted that the model originally showed high sensitivity to changes in Atlantic herring abundance, but this was attributed to model structure rather than a true ecological relationship (Anstead et al., 2021). The results from this investigation suggest that this omission should be reconsidered and that further research be dedicated to the effects of prey switching and alternate prey as management entities seek to incorporate ecological drivers into management plans across the Northwest Atlantic.

The linkages between longfin inshore squid consumption and Atlantic herring availability, combined with the known feeding ecology of Atlantic herring and longfin inshore squid, highlight a possibly complex dynamic between the two species. Indeed, longfin inshore squid may serve as both a competitor and predator to Atlantic herring, an alternative prey to higher trophic level predators of Atlantic herring including spiny dogfish, and both a predator and prey to themselves through cannibalism. As longfin inshore squid and Atlantic herring management entities consider ecological covariates in future management plans, incorporating these interactions may prove a challenging yet valuable area of research. Furthermore, as the distribution of spiny dogfish did not closely match any single prey species, future studies attempting to disentangle the ecological and environmental patterns of spiny dogfish distributions are warranted. As ocean conditions continue to change due to rising sea surface temperatures and associated climatological shifts, understanding habitat suitability and the ecological constraints of ecologically and economically important species, including spiny dogfish, will undoubtedly become increasingly important to the effective management of ecosystem services and living resources in the region.