During strong El Niño events, C. maenas and P. crassipes expanded their northern range via larval transport from the south. In their expanded range, crabs survive to adults, produce eggs and release viable zoea larvae. Due to selective tidal stream transport, larvae of both species released within most estuaries are transported to nearshore water for their pelagic development. Megalopae must migrate from coastal waters back to the shore or estuary. Why has C. maenas been able to established thriving self-maintaining populations on the west coast of Vancouver Island in just a few decades (Behrens Yamada and Gillespie 2008) after their introduction to San Francisco Bay, while P. crassipes, a native species, has not done so? The west coast north of Point Conception and the inland waters of British Columbia and Washington state have been viable habitats for adult P. crassipes at least since the end of the last ice age, yet in these roughly 10,000 years P. crassipes has not established self-sustaining populations in these locations. Contributing factors may be related to the timing of larval release, length of pelagic larval duration, and the circulation system to which the species is adapted.
Open Coast
Large populations of the Dungeness crab, Metacarcinus (Cancer) magister, are found within the California Current system from British Columbia south to Morro Bay, California. Like P. crassipes, M. magister has a long larval period (3 to 4 months), yet to date, self-sustaining populations of P. crassipes within the range occupied by M. magister have not developed. A major difference between the two species is the timing of larval release. Within the California Current, M. magister larval release is seasonal, occurring during winter months. The pattern of larvae release by M. magister is typical of shelf/slope fish and benthic crustacean species of the California Current system (Shanks and Eckert 2005). Shanks and Eckert hypothesize that this pattern of larval release/spawning coupled with a long PLD has evolved to capture the seasonal north south flow of the waters over the continental shelf as the currents shift from the winter northward flowing Davidson Current to the southward flowing California or Shelf-Break Current. By capturing this season shift in the flow, larvae may ultimately settle back into the extensive adult population of M. magister. The results of a coupled bio/physical model of M. magister larval dispersal is consistent with this hypothesis (Rasmuson 2013).
In the Southern California Bight, the pattern of P. crassipes megalopal return to the coast (peak returns Sept/Oct through March) suggests that, given a four-month larval development, larval release begins around May and continues through December, e.g., release starts in late spring, continues through summer and fall and ends at the beginning of winter. The extended period of larval release by P. crassipes is displayed by many fish and benthic crustacean species in the Southern California Bight (Shanks and Eckert 2005). Flow in the Bight is characterized by large, long-lived eddies; the extended spawning period may be an adaptation to this flow regime. Spawning in a similar pattern within the California Current system may, however, be maladaptive. Larvae released during the spring and summer by an imaginary population of P. crassipes on the Oregon coast would, during the 3 to 4 months of larval development, be carried far to the south by the steady flow of the nearshore Shelf-Current and offshore California Current; larvae would not be returned to this imaginary population. Larvae released around the fall transition in the winds (roughly mid October from southern BC to southern Oregon; (Thomson et al. 2014)) would be carried far to the north by the Davidson Current and these larvae also would not be returned to the spawning population. Larvae released in the winter that remained pelagic through the spring transition and the shift from the Davidson to the Shelf-break Current might be retuned to this imaginary population, but they would represent only a small proportion of the total reproductive output of the population. We hypothesize that this mismatch between the timing of larval release coupled with the long PLD and the seasonal hydrodynamics within the California Current prevents the establishment of self-sustaining populations of P. crassipes on the Pacific Northwest outer coast.
The larvae of a variety of species, mostly fish, typically found in the Southern California Bight are apparently transported northward out of the Bight during El Niño events and, like P. crassipes, they settle and establish ephemeral populations on the outer coast to the north of the Bight (Shanks and Eckert, 2005). The adults survive outside the Bight, but, likely because the mismatch of their spawning timing and PLD and the coastal hydrodynamics, self-sustaining populations have also not developed. If in the future, El Niño events become more frequent or the Davidson Current becomes stronger, then recruitment of larvae transported northward out the Bight might occur with enough regularity to sustain populations on the open coast outside the Bight. These would, however, likely not be self-sustaining populations as they would be dependent on recruits spawned in the Bight, but they could be much less ephemeral than current populations north of Coos Bay. The Davidson Current occurs each year, hence, there should be annual transport of larvae from the Bight some distance up the outer coast of California. These recruits may sustain populations on the outer coast some distance north of the Bight, i.e., north of Point Conception.
Retention on the west coast of Vancouver Island
We hypothesize that the systems of inlets along the west coast of Vancouver Island, stretching from Barkley Sound in the south to Quatsino Sound in the north, are strong candidates for range expansion of C. maenas, but likely not for P. crassipes. Some of the inlets and sounds have water residence times long enough that C. maenas larvae may be able to complete their development within the water body, but none of them have long enough residence time to maintain the P. crassipes larvae with their much longer PLD. Larvae of either species that are exported out onto the continental shelf will be transported by the northward flowing VICC. The PLD for C. maenas is short enough that the larvae may complete their pelagic development and migrate back to shore before they are carried north of Vancouver Island by the VICC. The months longer PLD of P. crassipes larvae likely would lead to their transport in the VICC to well north Vancouver Island.
Of the various sites along the west coast of Vancouver Island, Pipestem Inlet in northern Barkley Sound is the main water body where sustained populations of C. maenas have been observed (Graham Gillespie, pers. com; 2020). What is it about Pipestem Inlet that allows for populations of C. maenas but not P. crassipes? One immediately obvious reason for the retention of C. maenas in the inlet is that there is insufficient freshwater input from the small lake (Skull Lake) at the head of the inlet to generate a positive-type estuarine circulation, i.e., surface brackish outflow and compensating more saline inflow at depth. The Canadian Hydrographic Chart of Pipestem Inlet (No. 3670) shows that the entrance to the inlet (maximum depth of just over 60 m) is almost totally blocked by a series of islands (the Stopper Islands and Hillier and Snowden Islands) and by a shallow (~ 15 m) sill that impede tidal and estuarine exchange with the sea through Toquat Bay. These barriers will also limit circulation within the inlet. Equally importantly, the main freshwater flows that can affect circulation in the inlet – lake-fed Toquat River and Lucky and Cataract creeks – enter near the mouth of the inlet, rather than at its head. The hydraulic head produced by the freshwater discharge from these sources is directed radially outward from the source, i.e., seaward as well as into the inlet. Thus, the presence of freshwater discharge at the outer boundary of Pipestem Inlet could result in a negative (reverse) estuarine-type two-way circulation, with weak inflow at the surface and even weaker compensating outflow at depth. Locally, at least, there may be a mechanism for retaining larvae in the general vicinity of the inlet. Eastward blowing diurnal seabreezes that develop from late spring to early fall due to the air temperature contrast between the relatively warm land and cold water would help retain brackish water within the inlet, i.e., the seabreeze would push the brackish surface waters back up the inlet. The recirculation around the islands in Toquat Bay leading to Pipestem may help retain organisms just outside the inlet that may then enter/reenter with the “warm” brackish surface water during seabreeze wind conditions in Barkley Sound. Based on the hydrodynamics of Pipestem Inlet, there is a need to examine inlets with possible negative estuarine circulation arising from a combination of negligible runoff at their head and substantial runoff near their mouth.
Quayle (1988) lists inlets in British Columbia, where introduced Japanese oysters (Magallana gigas) reproduce naturally, and where shellfish growers can collect seed oysters. These inlets typically reach water temperatures > 18°C in the summer, allowing this warm temperate oyster species to mature, spawn, complete its planktonic development in ~ 1 month, and settle as seed oysters. On the west coast of Vancouver Island, these inlets include Pipestem Inlet in Barkley Sound and Tlupana Inlet in Nootka Sound. These are sites where C. maenas populations have been well established for over 10 years (Behrens Yamada and Gillespie 2008), and where P. crassipes have been found recently (Boulding et al. 2020). The flushing rate of these inlets and sounds is on the order of 2 months and thus long enough for C. maenas larvae to complete their development within the inlets and sounds. At water temperatures > 18°C the larval PLD is even shorter making retention more probable. The larvae of P. crassipes, however, would not be retained in these inlets because their planktonic development is 3–4 months and they would, thus, likely be flushed out to the open coast and not return to sustain the parental population. While these inlets served as incubators for C. maenas, we hypothesize that this is not the case for P. crassipes.
Retention in the Salish Sea
Gillespie et al. (2001) noted that many non-native mollusk species that are introduced into the Salish Sea take only a decade or so to spread throughout the Sea because their larvae are retained. This process may already be happening with C. maenas. Prior to 2010, a self-maintaining population of C. maenas was unintentionally introduced as hitch-hikers on mussels to Sooke Basin, northwest of Victoria. These mussels were collected from the west coast of Vancouver Island and stored in the inlet for biotoxin studies (Curtis et al. 2015). Densities of C. maenas built up quickly within Sooke Basin, but larvae from this population did not immediately start satellite populations in the Salish Sea. Due to the Coriolis force, the surface outflow from the Salish Sea is strongest along the Canadian side of Juan de Fuca Strait, in other words, right where the waters of Sooke Basint connect with the Straits of Juan de Fuca. This estuarine outflow of lower salinity water, fed by the Fraser and Skagit Rivers, flows out the Strait of Juan de Fuca most of the time (Thomson et al. 2017). C. maenas larvae make tidally timed vertical migrations, migrating into surface waters during ebb tide. This behaviour would tend to transport larvae out of the inland waters such as Sooke Basin and into the plume of estuarine waters flowing onto the continental shelf where the water mass turns northward becoming the VICC.
It was not until after the 2015–2016 El Niño and Pacific Heat Wave of 2014–2015 (The Blob Heat Wave) that C. maenas was discovered on the US side of the Salish Sea by members of Washington Sea Grant Crab Team, a consortium of volunteers, agency, tribal, University of Washington biologists and shellfish growers. Early sightings included Westcott Bay on San Juan Island, Padilla Bay, Dungeness Spit National Wildlife Refuge, Sequim Bay and Port Townsend Bay (Fig. 2, Grason et al. 2018, Brasseale et al. 2019). The proposed mechanism is the transport of larvae from the open coast into the Salish via the Olympic Peninsular Counter Current (Behrens Yamada et al. 2017). It is only during winter storms that strong southerly winds drive the surface water eastward along the southern shore of the Strait of Juan de Fuca into the Salish Sea. Most years the surface water temperature is below 10o C and not conducive for the development of C. maenas larvae. But during the winters of 2014–2015 and 2015–2016, water temperatures were warm enough (Behrens Yamada et al. 2017). Since then, C. maenas has been detected at various other locations on both the US and Canadian side of the Salish Sea (DFO AIS 2020, www.tinyurl.com/wagreencrab). The discovery of young-of-the-year crabs in high retention bays and lagoons (Buffington 2019, Mueller & Jefferson 2019) indicates local reproduction. Intense trapping efforts by Washington Sea Grant Crab Team, including Washington Department of Fish and Wildlife, the United States Fish and Wildlife Service, Padilla Bay National Estuarine Research Reserve, the Lummi Nation, the S’Klallam tribe, Taylor Shellfish and others are continuing. The goal is to reduce the breeding population in an attempt to prevent C. maenas from permanently establishing itself in the inland sea. For recent updates for Washington State sightings see: (https://wsg.washington.edu/crabteam/about/blog/ and www.tinyurl.com/wagreencrab)
As we have pointed out, P. crassipes has had the opportunity to colonize the Salish Sea since the end of the last ice age when the glaciers retreated from the area. In other words, they have something like 10,000 years to expand their range yet they have not. If we assume a strong El Niño every decade (roughly the current rate), then there may have been around 500 strong El Niño events during which P. crassipes larvae may have been transported into the Pacific Northwest. We hypothesize that the combination of the hydrodynamics of the Salish Sea with the biology of the crab prevents colonization. Flow throughout the Salish Sea is nearly continuously estuarine, i.e., surface flow is out of this large estuary. P. crassipes larvae within an estuary vertically migrate to exploit the seaward estuarine flow such that the larvae are transported onto the continental shelf. The long PLD provides enough time for the larvae to transit out of even this large estuary to the coast. This combination of hydrodynamics and larval biology may prevent P. crassipes from colonizing the Salish Sea via natural larval transport. However, if C. crassipes were to be transplanted into Hood Canal, a basin at the southern end of the Salish Sea (Fig. 2) with a water retention time of half to one year (Khangaonkar 2012), then a satellite population might establish. To test this prediction, we alert biologists to look for P. crassipes at other sites in the Salish Sea, and if they do, to document their sighting as range expansions.
Invasive Potential
A comparison of the range expansion of these two crab species may provide insight into the requirements for a species to be a successful invader. C. maenas is clearly a successful invader. In contrast, we are unaware of any reports of P. crassipes introductions and, as pointed out above, they have been unable to establish self-maintaining populations, even on the outer coast of Washington and northern Oregon, despite having literally thousands of years (if not much longer) in which to accomplish this. A disjunct Asian population of P. crassipes is found in Korea and Japan (Morris et al. 1980, Canepa & Terhorst 2019). Genetic analysis concluded that crabs from a Korean population were not introduced with shipping from the eastern Pacific, but that the two populations, on either side of the Pacific, diverged around one million years ago (Cassone & Boulding 2006). Furthermore, genetic analysis of populations sampled in California, Oregon, Washington and Bamfield, BC showed that these populations were not genetically distinct and that the Bamfield population did not exhibit reduced genetic diversity. These observations suggest that the gene pool of P. crassipes in the eastern Pacific is well mixed. We suspect that the difference in the invasion success between C. maenas and P. crassipes has to do with the pattern of coastal hydrodynamics to which their spawning and larval pelagic phase has evolved. Adult C. maenas is primarily estuarine-dependent, larvae are released within estuaries, but are exported to the coastal ocean where they go through their development. The megalopae migrate back to the shore and enter estuaries to complete their development. The hydrodynamics to which they have evolved are generic for many coasts; flow within estuaries and in the nearshore coastal ocean (i.e., within the coastal boundary layer) is very similar the world over. Hence, as the hydrodynamics to which they have evolved is common, we can think of their life history as being pre-adapted to many coastal settings. In contrast, we suspect that P. crassipes has evolved their spawning and larval pelagic phase to a unique hydrodynamics setting, the eddy filled Southern California Bight. The type of hydrodynamics present in the Bight is not common and this we suggest means that P. crassipes is pre-maladapted as an invader species nearly everywhere. They seem incapable of even establishing self-maintaining populations just to the north of the Southern California Bight.
What we are proposing is that the life history of a species coupled with the hydrodynamic setting in which their pelagic larvae develop will determine a range expansion. If we compare the northward and southward range expansion of C. maenas out of San Francisco Bay we can actually see an example of this. During the El Niños, the range of C. maenas expanded rapidly northward such that they are present in Canada; a range expansion of about 1,500 km. Over the same period, they have expanded to the south only as far as Elkhorn Slough in Monterey Bay; a range expansion of only 150 km. Why do we see a factor of 10 difference in their range expansion? A likely explanation is the timing of larvae release (Jan-March in Coos Bay, Oregon) coupled with the hydrodynamics of the coastal ocean during that period; flow is primarily to the north as the Davidson Current. The southward flowing California Current does not ‘return’ to the shelf waters until after the shift from the winter northward winds to the spring summer southward winds, the spring transition, which on average occurs in mid April. Nearly all of the larvae leaving San Francisco Bay travel north in the Davidson Current. Larvae released after the spring transition will travel to the south in the California Current, but given the available data on larval release it looks like only a small percentage of larvae will be carried south. A tiny population has established in Elkhorn Slough (Grosholz 2011). What happens to their larvae? Given the timing of larvae release nearly all will go north and the very few larvae from this tiny population that are released after the spring transition must be carried past the coast of Big Sur (≈ 200 km) before they might arrive at another small estuary (Morro Bay). Life history coupled with coastal hydrodynamics appears to be determining range expansion.