Oceanographic changes and the distribution and abundance of southern taxa

Although shifts in geographic distribution have frequently been associated with strong El Niño events21,22,26,48 and other marine heatwaves49, the number of poleward range extensions observed during this study appears unprecedented. Conditions in northern California during 2014–2016 were characterized by SST that were often 2–4 °C above the climatological mean, and included a series of more than a dozen heatwaves (i.e., events lasting ≥5 days with SSTs warmer than the 90th percentile based on the 30-year climatology1). The most intense heatwave at Bodega Bay lasted 199 days (August 2014 to late February 2015), with a cumulative intensity (518.3 °C days) that exceeded that of other extreme heatwaves recorded in Western Australia (2011), the NW Atlantic (2012), the Mediterranean Sea (2014), and the Tasman Sea (2015–2016)1,50. Given that cooler SST can limit the development and successful recruitment of larval stages of biota from lower latitudes43,51, the unusually long duration of anomalously warm temperatures in northern California during 2014–2016 was likely a primary driver of poleward range shifts observed in our study.

In addition, anomalous poleward transport might have contributed to shifts in the distribution of southern biota during 2014–2016, a hypothesis proposed to explain geographic range expansions during some previous El Niño events21,23,52,53. Larval dispersal is influenced by a combination of advective and diffusive processes54, both of which may be important in explaining poleward transport in our study. Alongshore currents during 2014–2016 exhibited anomalous poleward flows, especially during the second half of 2014. Although such anomalies were infrequent overall, the persistent 15 cm/s poleward flow past Point Año Nuevo during November 2014 could have advected plankton over distances of ~500 km in one month. Moreover, it is possible that some plankton were transported north through a sequence of poleward flows rather than a single advection event. During late 2014, alongshore flow often did not revert to equatorward flow between poleward flow anomalies. This pulsed advection, such as the stop-start poleward flow past Point Año Nuevo during July–August 2014, can account for ~300 km displacement. Lastly, poleward transport might arise via a diffusion mechanism in which some of the plankton transported north during a brief event are not returned south as flows reverse, but are retained and transported farther north during the next brief poleward event. This process might ultimately result in a portion of the larval pool moving considerable distances north through a series of poleward flow events, such as flows past Point Reyes during July–October 2014 (potential displacement of ~400 km). This last diffusive transport scenario can be enhanced by retention features like bays (e.g., Monterey Bay, or the Gulf of Farallones) or offshore mesoscale eddies and requires that some flows be directed poleward, especially from March to August when mean flow off central and northern California is typically equatorward. Thus, even marginally anomalous flows, as observed during 2014–2016, might result in a marked increase in the probability of poleward transport of propagules.

There are other possible explanations for anomalous transport of warm-water biota into our region during 2014–2016. In particular, enhanced onshore transport might have delivered organisms to coastal waters that are typically found in warmer, offshore waters, including many of the pelagic species reported in this study. Although there was no evidence of anomalous downwelling along the California coast during 2014–201615, previous studies suggest additional mechanisms of onshore transport during El Niño years55.

It is likely that both temperature and transport played a role in the poleward shift of biota, and that the combination of these effects would be more effective than either one alone41,42,56. For example, warmer temperatures shorten planktonic larval durations57 and thus may increase the chances that southern species will be transported poleward, complete development, and settle in benthic habitats within the timespan of temporary current reversals51,58. Indeed, the combined influence of changes in temperature and currents has facilitated range expansions in other geographic regions8,9,41,42,43,56,59.

While we recorded range extensions and/or increased recruitment of many southern species, others species with northern range boundaries at Monterey Bay did not undergo range expansions into our study region. Individualistic responses of this kind have been observed in other studies of geographic range shifts and likely depend in part on the specific life histories, dispersal potentials, and habitat requirements of a given species39,42,60,61. For example, many of the nudibranch species in our study reproduce over a large proportion of the year, including production of larvae during fall and winter (Table S4). Similarly, the larvae of owl limpets and volcano barnacles both occur in the plankton primarily during the second half of the year (September–January, and July–November, respectively62,63). The timing of larval dispersal in these species thus overlapped with periods of strong surface poleward flow and warm SST during 2014–2016 (Figs 2 and 3). In contrast, planktonic larvae of species that reproduce during the spring likely encountered primarily equatorward flow and more typical, cooler SST during 2014–2016.

The magnitude of geographic range extensions was greatest for taxa that are members of the pelagic community as adults (e.g., jellyfish, ctenophores, pteropods, and pelagic red crabs). The prolonged occurrence of these species in the pelagic environment presumably increases the chances that some individuals will be transported poleward by advective and diffusive processes. For benthic taxa that experienced range extensions, species with planktonic, feeding larvae exhibited greater range extensions than those species with direct development and limited dispersal potential, such as brooding sea cucumbers. Although some meta-analyses have found faster range extensions in pelagic organisms and highly mobile fish than in benthic species64, others have failed to find a significant effect of reproductive mode and dispersal potential on the rate of range shifts65,66. When evaluated over the same timescale as anomalous conditions during 2014–2016, dispersal potential likely had a direct influence on the colonization of poleward regions. In contrast, when range shifts are assessed over decadal timescales65,66, initial patterns of dispersal and colonization during heatwaves may sometimes be reshaped by additional abiotic and biotic factors.

Persistence of ecological changes

Ecological changes associated with marine heatwaves can lead to population changes that range from short-lived to persistent9,67. Poleward appearances of southern biota beyond their typical range boundaries are often ephemeral, with species disappearing from the region when the oceanographic event ends, due to unsuitable conditions in the northern habitat and/or the short lifespan of some species53. This was the case, for example, for many of the primarily southern nudibranchs that occurred only ephemerally in our study region during the marine heatwaves (e.g., Flabellinopsis iodinea, Anteaeolidiella oliviae, Janolus barbarensis, and others20). In other cases, larval recruitment may establish “relict populations” that decline in abundance more slowly before eventually disappearing67. This may be the case for the Hopkins’ Rose Nudibranch (Okenia rosacea), which was still present in northern California during summer 2018, over two years after the El Niño ended, but at much lower densities than occurred in the region during 2015–2016 (see Supplementary Information). A final possible outcome of marine heatwaves is that warmer water and increased larval transport from lower latitudes may establish or sustain “marginal” or sink populations that can persist indefinitely67. Such sink populations are maintained primarily by episodic larval recruitment from southern source populations68, as appears to be the case for owl limpets and volcano barnacles in our study region63,69.

Whether or not northern populations established during marine heatwaves persist will likely be influenced by several other factors beyond future larval recruitment and connectivity with southern source populations. First, the physiological tolerances of a species will determine if new recruits can persist in poleward habitats when more typical temperatures return42,51,56,59. Second, the lifespan of a species will also influence the persistence of marginal populations. For example, volcano barnacles and owl limpets are relatively long-lived species, and individuals can live 10–15 years62 or >20 years69, respectively. Moreover, our results suggest that survival of juvenile owl limpets in northern California is relatively high. Thus, even infrequent recruitment associated with El Niño events may be sufficient to maintain marginal populations of some southern species68,69. Finally, mode of reproduction and habitat are likely important in determining whether marginal populations will contribute to future recruitment in the northern region. For example, for broadcast spawners, low population density may reduce fertilization success via Allee effects39. Open coast populations that produce planktonic larvae near the northern edge of a geographic range might contribute minimally to future recruitment in this region if prevailing coastal currents carry most larvae equatorward58. In contrast, species with direct development (e.g., brooders) might be self-sustaining once a sufficiently dense population is established in a northern location. During our study, two species with direct development (Lissothuria nutriens, Petaloconchus montereyensis) underwent striking increases in local abundance in northern populations (see Supplementary Information). The capacity for self-recruitment may allow southern species with direct development to respond rapidly to favorable, warm-water conditions.

Range expansions in a temperate transition zone

Temperate transition zones are often hotspots of diversity because these regions contain a mix of both warm-adapted and cool-adapted species37,39. The coast of California from Monterey Bay to Point Arena represents such a transition zone with high species richness that arises in part from benthic communities that include a mix of species with differing biogeographic affinities5. For example, of the 10 common intertidal barnacles in California, two are cosmopolitan species found coastwide, four are primarily northern, and four are primarily southern34. All 10 species occur in the region from Monterey Bay to Point Arena, and the boundary of this transition zone has shifted poleward since the 1970s (Fig. 6). Although El Niño events are typically viewed as ecological disturbances, not all associated effects on marine ecosystems are negative70. Indeed, episodic periods of warmer water and enhanced northward transport during warm-water events may be critical to the recruitment and population persistence of some primarily southern species in northern California. This may be particularly true for relatively long-lived species where northern populations can persist through extended periods of low recruitment. These recruitment dynamics may play an underappreciated role in maintaining the high species richness of transition zones. For example, during 2014–2016, all four southern barnacles in our study region increased in abundance and/or experienced geographic range extensions.

Figure 6 Geographic ranges of common intertidal/shallow subtidal barnacles of California (after Newman34). This assemblage includes species that are cosmopolitan (black bars), primarily northern (blue bars), and primarily southern (red bars). The highest species richness of intertidal barnacles occurs in central/north central California between Point Conception and Point Arena. For southern species, red bars indicate northern range limits during the 1970s34, and dark red bars indicate geographic range expansions to current poleward boundaries (see Supplementary Information). Species are coded as follows: (1) Pollicipes polymerus, (2) Balanus glandula, (3) Chthamalus dalli, (4) Balanus nubilus, (5) Balanus crenatus, (6) Semibalanus cariosus, (7) Paraconcavus pacificus, (8) Chthamalus fissus, (9) Tetraclita rubescens, (10) Megabalanus californicus. Note that southern range limits are those published by Newman34, as we are unaware of data that address whether these equatorward boundaries have retracted. Full size image

Episodic recruitment of southern species during El Niño events may also play a key role in facilitating geographic range expansions against a backdrop of ongoing climate change. In recent decades, the species composition of intertidal communities in the Bodega Bay region has shifted to include more southern fauna of the Montereyan biogeographic province, including the sea anemone Anthopleura sola, the barnacles Tetraclita rubescens and Megabalanus californicus, the porcelain crab Petrolisthes manimaculis, the owl limpet Lottia gigantea, and the vermetid tube snail Thylacodes squamigerus. These six species were historically rare or absent in the region during the 1970s (see Supplementary Information), but all have become more common in recent decades, including marked increases in abundance during 2014–2016. In addition, the geographic ranges of four of the six species expanded farther north during 2014–2016. Our results are thus consistent with a gradual shift in the poleward boundary of the Montereyan biogeographic province5 analogous to trends towards tropicalization seen in other regions of the world8,37,39.

Growing evidence suggests that gradual, long-term shifts in geographic distributions can be punctuated by rapid expansions where marginal populations are established during extreme events6. Meta-analyses suggest that marine range extensions have occurred at a mean rate (±SE) of 72.0 km (±13.5) per decade64. In contrast, the mean (±SE) range extension recorded in our study was 345.4 km (±53.9 ) occurring within a period of a few years or less. Thus, marine heatwaves provide a mechanism for the rapid poleward expansion of some species into new regions. While many of these northern populations might not persist, the establishment of such marginal populations may be essential if poleward range expansions proceed in a stepping-stone fashion71. Marginal populations established during extreme events might be more likely to persist if background levels of ocean warming make northern habitats more favorable for southern species during intervening periods between these events59. In addition, more frequent and longer heatwaves might also increase the persistence of marginal populations and accelerate shifts in species ranges37. For example, the prolonged duration of warm-water conditions and two years of successful larval recruitment might have allowed populations of volcano barnacles, owl limpets, and other southern species to reach a threshold density for effective reproduction (e.g., a minimum density required for fertilization success in broadcast spawning limpets or copulating barnacles). Our surveys of owl limpets in May 2018 indicate low levels of larval recruitment occurred in northern California in late 2016 after warm-water conditions had dissipated. This suggests the possibility that owl limpet populations in our study region have become sufficiently dense that they are starting to contribute larvae that may help sustain northern populations and perhaps facilitate a poleward shift in geographic distribution.

Whereas relatively short, high-intensity marine heatwaves can be sufficient to trigger mass mortality events1,7, we suggest that greatly prolonged heatwaves, like those that occurred along the California coast during 2014–2016, are especially likely to facilitate poleward dispersal and range extensions. Understanding the oceanographic, ecological, and evolutionary processes that mediate the success of such range expansions will be critical to predicting future shifts in the community composition of biogeographic transition zones in an era of accelerating climatic change.