The Savory Swimmer Swims North: A Northern Range Extension of the Blue Crab Callinectes Sapidus?

Abstract

Worldwide, climate-change is shifting species distributions poleward. Here I present recent (2012-2014) observations of the blue crab, Callinectes sapidusRathbun, 1896, in the Gulf of Maine (GoM), north of its historical range of Cape Cod, Massachusetts. To test the hypothesis of a climate-driven range expansion, I examined near-surface ocean temperatures. On average, ocean temperatures in the GoM in summer 2012 and 2013 were up to |$1.3^\circ{\rm{C}}$| higher than the average of the previous decade, suggesting that warmer waters may have promoted the recruitment of C. sapidus to the GoM. Previous ephemeral populations of C. sapidus in the Gulf of Maine have been reported since the 1860s. Recent observations and continued warming in the northwest Atlantic may signal a permanent poleward expansion of C. sapidus into the GoM. If so, then a key goal for ecologists and managers will be to understand the effect of C. sapidus on GoM food-webs and fisheries.

Introduction

A consequence of climate change is a shift in species distributions (Groffman et al., 2014; International Panel on Climate Change, 2014). In the world’s oceans, the distributions of warm-water marine fishes and invertebrates are shifting poleward (Perry et al., 2005; Lucey and Nye, 2010; Cheung et al., 2013; Poloczanska et al., 2013; Johnson, 2014), a trend that is positively correlated with increasing global ocean temperatures (Cheung et al., 2013). In recent years, the northeast United States sea-surface temperatures have increased |$0.1^\circ{\rm{C/decade}}$| (Belkin, 2009). As a result of this warming, warm-water ocean species – including commercially important species – are rapidly occupying formerly cold-water provinces (Lucey and Nye, 2010; Johnson, 2014), which has important ecological and economic implications (Fogarty and Lipcius, 2007; Pinsky and Fogarty, 2012).

The blue crab, Callinectes sapidusathbun, 1896 is a commercially important and warm-water decapod. Its historical northern limit is Cape Cod, Massachusetts (Fig. 1, Burbanck, 1962; Williams, 1974; deRivera et al., 2005); though some literature and field guides consider its range to extend as far as Nova Scotia (Gosner, 1978). This may result from the reports of ephemeral populations of C. sapidus in the Gulf of Maine (GoM) since the 1860s (Cooke, 1867; Piers, 1923; Scattergood, 1960). Although blue crabs are occasionally found as far north as Nova Scotia, year-round populations historically have only existed from Massachusetts southward (Williams, 1974; deRivera et al., 2005). Thus, I do not consider the GoM as part of historical range of C. sapidus because no permanent populations of C. sapidus have yet been established.

Fig. 1

Historic geographic distribution of Callinectes sapidus and possible range extension (dashed line) on the east coast of the United States. Arrows indicate location of C. sapidus observed in 2012-2014 in the Gulf of Maine. Basemap provided by United States Geological Society’s National Map Viewer (http://viewer.nationalmap.gov/viewer/). This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/journals/1937240x.

In 2012, a newspaper reported the collection of C. sapidus 100 km north of Cape Cod in Marblehead, Massachusetts (Daily News, 2012). As sea temperatures have risen in the GoM (Belkin, 2009), this newspaper report may be the first record of the northern movement of C. sapidus associated with climate change. Additionally, colleagues at the Plum Island Long-Term Ecological Research site in northeast Massachusetts, reported observations of C. sapidus to the author in 2012 (Jimmy Nelson, Evan Howard and Chris Haight, personal communication). Thus, the objectives of the current study were to: 1) document recent (2012-2014) observations and collections of C. sapidus in the GoM, 2) establish the northern extent of the historical range of C. sapidus, and 3) examine water temperature as a potential driver of the recruitment of C. sapidus in the GoM.

Materials and Methods

To document observations of C. sapidus in the GoM, I queried scientific colleagues and conducted a member survey of the New England Estuarine Research Society list-serv in 2013 and 2014 and followed up on any reports or suggested contacts.

To confirm the presence of C. sapidus in the GoM I conducted annual field surveys in August of 2012-2014 in saltmarsh tidal creeks in the Plum Island Estuary (PIE) in northeastern Massachusetts, where sightings of C. sapidus had been reported. The PIE is a macro-tidal (2.5 mean tidal range) estuary dominated by salt marshes behind a barrier island. The selected tidal creeks are part of routine invertebrate sampling by the PIE-Long-Term Ecological Research (PIE-LTER) program and no C. sapidus have been reported in the past 20 years of routine annual surveys in the broader estuary and in the tidal creeks using various methods (e.g., flume nets, beach seines) (Deegan et al., 2007; Johnson and Fleeger, 2009; http://pie-lter.ecosystems.mbl.edu/content/dynamics-populations). The dominant common decapods in these tidal creeks are sand shrimp, Crangon septemspinosaSay, 1818; grass shrimp, Palaemonetes pugioHolthuis, 1949; and green crabs, Carcinus maenas (Linnaeus, 1758) (cf. Deegan et al., 2007).

Annual surveys were conducted in six tidal creeks distributed throughout the estuary by walking along |$250\,{\rm{m}}$| of creek bottom at low tide and jabbing the sediment with a long-handled net to disturb any benthic animals. All collected C. sapidus were measured for maximum carapace width (from lateral spine to lateral spine).

Generally, Cape Cod is considered the northern limit of C. sapidus (Burbanck, 1962; Williams, 1974; deRivera et al., 2005), although there have been historical observations of blue crabs in the Gulf of Maine (Cooke, 1867; Piers, 1923; Scattergood, 1960). To determine if there have been more recent observations of C. sapidus in the GoM, I conducted a Web of Science (a citation index of strictly peer-reviewed literature provide by Thomas Reuters) search from 1955 to 2013 with the search terms ‘blue crab^∗’ or ‘Callinectes’ in combination with and ‘Maine’ or ‘Gulf of Maine’ or ‘Canada’ or ‘New Hampshire’ or ‘Nova Scotia.’ A world-wide web (Google) search was also conducted using these terms for potential ‘gray literature’ (e.g., government reports) sources.

To determine if water temperature may be a possible driver of a C. sapidus range expansion, I examined near-surface |$({\text{1-m depth}})$| ocean temperature data from 2001-2013 in Massachusetts Bay (Station 44029, Buoy A01) and the Central Maine Shelf (Station 44032, Buoy E01). Data courtesy of the Northeast Regional Association of Coastal and Ocean Observing Systems (http://www.neracoos.org).

Results

Anecdotal evidence (reports from shellfish wardens and wildlife managers) suggests that C. sapidus were observed in Duxbury Bay and Marblehead, Massachusetts, NH, USA, New Meadows Lakes, ME, USA, and Little Port Joli Estuary, NS, Canada, in 2012 (Daily News, 2012; Derek Perry, Dan Devereaux and Chris McCarthy, e-mail communication; Table 1). In 2013, C. sapidus was observed in New Meadows Lakes, ME, USA (Dan Devereaux and Linda Mercer, e-mail communication). In May 2014 C. sapidus was observed in Little Port Joli Estuary, NS, Canada (Chris McCarthy, e-mail communication).

Table 1

Observations of Callinectes sapidus north of Cape Cod, MA, USA in 2012-2014.

Location (from S to N)	Latitude (N)	Longitude (W)	Habitat	Observation date	Carapace width (cm)	Reference
Historical observations |$(\lt2012)$|
Salem Sound, MA,	|$42^\circ29'37''$|	|$70^\circ53'26''$|	A salt pond	1867	|$-$|	Cooke (1867)
USA Cow Bay, Halifax, NS, Canada	|$44^\circ37'3''$|	|$63^\circ25'39''$|	–	1902-1903	10.7-15.3	Piers (1923)
Knox County, ME, USA to Portsmouth, NH	|$44^\circ6'12'' {\text{-}} 43^\circ4'23''$|	|$69^\circ3'33'' {\text{-}} 70^\circ44'44''$|	–	1948-1956	12.7-19.1	Scattergood (1960)
Port Maitland, NS, Canada	|$43^\circ59'16''$|	|$66^\circ9'45''$|	–	1953	18.0	Scattergood (1960)
Sheepscot River, ME, Canada	|$43^\circ47'49''$|	|$69^\circ41'50''$|	–	1977	17.3-17.9	Krouse (1979)
Recent observations (2012-2014)
Duxbury Bay, MA, USA1	|$42^\circ1'32''$|	|$70^\circ40'3''$|	Estuary	Fall 2012	|$\gt12$|	This study
Marblehead, MA, USA2	|$42^\circ30'32''$|	|$70^\circ50'23''$|	Seagrass	July 2012	|$-$|	This study
Plum Island Estuary, MA, USA3,4	|$42^\circ43'54''$|	|$70^\circ50'9''$|	Saltmarsh tidal creek	August 2012, 2014	8.1-9.1	This study
New Hampshire5	|$43^\circ1'32''$|	|$70^\circ42'7''$|	Estuary	Summer 2012	|$-$|	This study
Little Port Joli Estuary, NS, Canada6	|$43^\circ51'45''$|	|$64^\circ48'47''$|	Mud	September 2012, May 2014	7.5-12.5	This study
New Meadows Lake, ME, USA7,8	|$43^\circ55'13''$|	|$69^\circ51'53''$|	Mud	Fall 2012/2013	|$-$|	This study

¹

Photographic evidence of molts presented to Derek Perry of Massachusetts Division of Marine Fisheries.

²

Reported by the Daily News newspaper 4 August 2012.

³

2012 specimens collected by author.

⁴

2014 specimen observed by Olivia Bernard.

⁵

An oral report provided to Derek Perry, MA, USA Division of Marine Fisheries.

⁶

Observed directly by Chris McCarthy of Parks Canada, NS, Canada.

⁷

Specimen presented to Dan Devereaux, Marine Steward of Brunswick, ME, USA, by a quahog (Mercenaria mercenaria) harvester.

⁸

Oral report to Linda Mercer of the Department of Maine Resources.

I confirmed the presence of C. sapidus in the GoM in 2012 when I collected four C. sapidus individuals with a carapace width of |$8.1{\text{-}}9.1\,{\rm{cm}}$| in the PIE tidal creeks (Fig. 2), which is smaller than the crabs found in previous reports (⁠|$10{\text{-}}18\,{\rm{cm}}$|⁠, Table 1) of blue crabs in the GoM. I found no C. sapidus in 2013 or 2014 with the tidal creek surveys. On 2 July 2014, however, an individual C. sapidus was observed and hand-caught by intern Olivia Bernard but not retained. She described it as having large lateral spines, blue legs and claws, being very aggressive; all characteristics consistent with C. sapidus. This crab was just smaller than her hand (which is |$9.5\,{\rm{cm}}$| wide), consistent with the size of crabs collected in 2012 in the PIE tidal creeks.

Fig. 2

A blue crab (Callinectes sapidus) caught in Sweeney Creek by the author in the Plum Island Estuary, MA, USA, in August 2012.

Based on yearly averages, water temperatures in Massachusetts Bay were |$1.3^\circ{\rm{C}}$| higher in 2012 and |$0.7^\circ{\rm{C}}$| higher in 2013 than the mean of 2001-2013 water temperatures combined (Fig. 3). A similar water-temperature trend was seen for the central Maine shelf (Buoy E01; data not shown).

Fig. 3

Water temperature data |$1\,{\rm{m}}$| below the surface of Massachusetts Bay (Buoy A01). Solid black line represents monthly mean temperature. Dashed white line represents monthly mean data averaged across years 2001-2013. Gray band represents monthly maximum and minimum temperatures recorded from 2001-2013. Data courtesy of Northeast Regional Association of Coastal and Ocean Observing Systems (http://www.neracoos.org).

A Web of Science search revealed no reports in the recent peer-reviewed literature of C. sapidus in the GoM since Scattergood’s 1960 report. A World Wide Web search revealed a report of C. sapidus in the GoM in which two C. sapidus (⁠|$\geqslant17.3\,{\rm{cm}}$| carapace width) were collected in Sheepscot Estuary, Maine in 1977 (Krouse, 1979).

Discussion

Recently, C. sapidus has been observed in the Gulf of Maine to at least Nova Scotia, which is 500 km north of its historic range of Cape Cod, Massachusetts. Given that no reproductive females were reported and the observations were inconsistent due to low crab abundance, it is unknown if this population is an ephemeral one like those previously reported (Scattergood, 1960) or the beginning of permanent population. Furthermore, a true range extension is the result of a permanent population establishing in novel habitats. The three years of observations/anecdotal reports from this study are not enough to determine if the population has established. For instance, Scattergood (1960) reports C. sapidus observations in the GoM for 9 years beginning in 1948, with none after 1956. The observations in the current study are nonetheless valuable either to: 1) establish the genesis of permanent C. sapidus population in the GoM and thus a range extension, or 2) to note the continued phenomena of the occasional sojourn of C. sapidus into the GoM.

In either case, the recent observations of C. sapidus into the GoM are likely the result of increasing ocean temperatures. During the summers of 2012 and 2013 ocean temperatures were up to |$1.3^\circ{\rm{C}}$| higher than the average of the previous decade. Thus, warmer waters may have facilitated the recruitment of C. sapidus in the GoM. Historically, C. sapidus observations in the GoM have been attributed to warmer than usual ocean temperatures (Scattergood, 1960). While sporadic reports of C. sapidus in the GoM have occurred since the 1860s (Cooke, 1867; Piers, 1923; Scattergood, 1960; Rouse, 1979), the recent observations documented in this study and a trend of steadily increasing ocean waters in the northeast United States (Belkin, 2009; Lucey and Nye, 2010), may signal the northern expansion of C. sapidus into the GoM. Similarly, the fiddler crab Uca pugnax (Smith, 1870) also exhibited a northern range expansion recently (Johnson, 2014).

It is unknown if these crabs recruited to the GoM as swimming adults or settled larvae. Much work has been conducted on the thermal tolerances of different life-stages of mid-Atlantic C. sapidus (Tagatz, 1969; Schaffner and Diaz, 1988; Bauer and Miller, 2010), but it would serve to conduct rigorous studies on the most northern (Cape Cod) populations – the likely source of GoM crabs – to elucidate how temperature may drive an expansion of C. sapidus into the GoM (Sanford et al., 2006). Based on the information available, I present a number of hypotheses.

Callinectes sapidus larvae have been captured in plankton tows on the Scotian Shelf in the GoM (Roff et al., 1984) suggesting current transport of C. sapidus larvae, like other warm-water crustacean species, into the GoM is possible. In the fiddler crab, U. pugnax, the northern limit is set by thermal tolerances of larvae and not by adults (adults can overwinter in sites north of their range) (Sanford et al., 2006). Uca pugnax now has an extended range into New Hampshire possibly due to settlement of larvae during the warmer-than-average summer temperatures of 2012 and 2013 (Johnson, 2014).

Larval recruitment, however, may have not been the vector for C. sapidus recruitment to the GoM. The lower limit of larval development of mid-Atlantic crabs is |$19^\circ{\rm{C}}$| (Sandoz and Rogers, 1944). The collection, however, of |$\gt8.1{\text{-cm}}$| carapace width crabs in Massachusetts in 2012 suggests an age of at least one year (Puckett, 2006), suggesting crabs recruited as early as 2011, a year when highest mean summer temperature, the time of larval dispersal, was |$18.7^\circ{\rm{C}}$|⁠. Though it is possible that cold-adapted larvae may have developed at these temperatures.

Alternatively, the warmer-than-average winter temperatures of 2012 and 2013 may have allowed juvenile crabs to recruit into the GoM. Juvenile crabs have high winter-survivorship in bottom-water temperatures as low as |$0{\text{-}}5^\circ{\rm{C}}$| (Tagatz, 1969; Rome et al., 2005; Bauer and Miller, 2010), though small crabs |$(\lt30\, {\rm{mm}})$| experience high mortality at temperatures |$ \lt\,3^\circ{\rm{C}}$| (Rome et al., 2005; Bauer and Miller, 2010). In this scenario, crabs would have made movements into the GoM in the late summer/fall ahead of the warmer winter and buried in the mud or moved into deeper waters to overwinter (Schaffner and Diaz, 1988). Adult crabs may have recruited as well, though mature females experience high winter mortality at temperatures |$\lt\,5^\circ {\rm{C}}$|⁠.

An alternative hypothesis is that the populations of C. sapidus observed in the GoM may be a result of genetic selection for cold-tolerant individuals (Dennis and Hellberg, 2010). While no genetic analyses were conducted on these crabs, it is unlikely that there was genetic selection for cold-tolerant species because the expansion seems to have happened quickly (a movement of 500 km in two or three years). Furthermore, in studying the recent invasion of the mud fiddler crab, U. pugnax, into the GoM, Sanford et al. (2006) found that gene flow between northern and southern population was sufficient to swamp out any selection for cold-tolerant crabs. This may also be the case for C. sapidus.

The Atlantic Multidecadal Oscillition (AMO) is an index of climate variability in the north Atlantic and can shift species boundaries (Nye et al., 2013) and influence C. sapidus abundances (Colton et al., 2014). The AMO is typically expressed as variability in sea-surface temperature, also includes alterations in ocean circulations and primary production, which may have also influenced the recruitment of C. sapidus to the GoM in conjunction with warmer temperatures lowering physiological barriers.

An ecological hypothesis is that C. sapidus routinely enter the GoM but are thwarted via biotic resistance due to encounters with competitors, e.g., green crabs, Carcinus maenas (MacDonald et al., 2007) and predators, e.g., striped bass, Morone saxatilis (Overton et al., 2009). This hypothesis suggests that in recent years the interactions with these enemies was suppressed and allowed C. sapidus to persist.

Regardless of the mechanism of recruitment for C. sapidus into the GoM, the observations of C. sapidus in the GoM over multiple years suggests these crabs may be establishing. If C. sapidus, like many marine species, are tracking climate change (Pinsky et al., 2013) and ocean waters continue to warm as predicted (International Panel on Climate Change, 2014), then we can expect to see increases in their abundances as their populations establish in the GoM. Furthermore, the possible expansion of C. sapidus into the GoM represents a biological invasion. Marine ecosystems just poleward of current warm-water species ranges may be the most vulnerable to invasion as a result of climate-driven range expansions/shifts. Given that global temperatures continue to increase (International Panel on Climate Change, 2014) and that climate-change induced range shifts in fishes and crustaceans have been documented worldwide (Perry et al., 2005; Lucy and Nye, 2010; Poloczanska et al., 2013), we can expect the number of these invasions to increase (Sorte et al., 2010; Poloczanska et al., 2013; Johnson, 2014).

Range shifts can affect fisheries as commercially important species shift or expand their historical ranges (Lucey and Nye, 2010; Poloczanska et al., 2013). A C. sapidus expansion into the GoM may have byzantine economic and ecological consequences. While C. sapidus itself is a harvestable species, it can impact other harvested species, particularly bivalves, which represent a multi-million-dollar shellfishery in New England (Brousseau, 2005; Congleton et al., 2006). For instance, C. sapidus is a major predator of the commercially important soft-shelled clams, Mya arenaria (Seitz et al., 2005) and may negatively impact that shellfishery. At the same time, C. sapidus may benefit bivalve fisheries. The invasive European green crab (Carcinus maenas) has an estimated negative impact on the New England soft-shell clam fishery of $44 million/year (Lafferty and Kuris, 1996). Callinectes sapidus is a major predator of C. maenas and at high enough densities can limit green crab populations (deRivera et al., 2005). Thus, if we are seeing a true range expansion of C. sapidus into the GoM, a key question for ecologists and managers is what the net effect of C. sapidus on current GoM coastal food-webs and fisheries will be.

Acknowledgements

I thank Derek Perry, Chris McCarthy, Linda Mercer and Dan Devereaux for responding to my emails. I thank Jimmy Nelson, Chris Haight, and Evan Howard for their initial reports of blue crabs in Plum Island. I thank David Kimbro and Jarrett Byrnes for encouraging me to write these observations up for publication. I thank Richard Heard for confirming Callinectes sapidus identification. Comments from John Fleeger, Tom Trott and Lawrence Rozas, and two anonymous reviewers improved this manuscript. This work was funded by NSF Grants No. 1354494 and 1238212. Additional support from the Northeast Climate Science Center, Grant No. DOI G12AC00001.