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PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES
Series 4, Volume 65, No. 3, pp. 107–131, 13 figs., 2 tables September 28, 2018
Heterobranch Sea Slug Range Shifts in the Northeast Pacific
Ocean associated with the 2015-16 El Niño
Jeffrey H. R. Goddard 1, Nancy Treneman 2, Tara Prestholdt 3, Craig Hoover 4,
Brenna Green 5, William E. Pence 6, Douglas E. Mason 7, Phillip Dobry 8,
Jacqueline L. Sones 9, Eric Sanford 10, Robin Agarwal 11, Gary R. McDonald 12,
Rebecca F. Johnson 5, Terrence M. Gosliner 5
1Marine Science Institute, University of California, Santa Barbara, CA 93106-6150; email:
jeffg@ucsb.edu. 2Oregon Institute of Marine Biology, University of Oregon, Charleston, OR 97420.
3Department of Biology, The University of Portland, 5000 N Willamette Blvd, Portland, Oregon 97203.
4Department of Biological Sciences, California State Polytechnic University, 3801 W. Temple Ave.,
Pomona, California 91768-4032. 5Department of Invertebrate Zoology and Geology, California
Academy of Sciences, 55 Music Concourse Dr., Golden Gate Park, San Francisco, CA 94118-4503.
625 Tarabrook Dr., Orinda, CA 94563. 7Science Department, California High School, San Ramon, CA
94583. 8 33 Petar Place, San Ramon, CA 94583. 9Bodega Marine Reserve, University of California,
Davis, P.O. Box 247, Bodega Bay, CA 94923. 10 Department of Evolution and Ecology, University
of California, Davis, Bodega Marine Laboratory, P.O. Box 247, Bodega Bay, CA 94923.
11 3114 Flowers Lane, Palo Alto, CA 94306. 12 Long Marine Lab, University of California
Santa Cruz, 100 Shaffer Road, Santa Cruz, CA 96050
The strong 2015–16 El Niño comprised the second part of the unprecedented 2014–
17 marine heat wave in the Northeast Pacific Ocean. From late 2015 through 2017
we sampled mostly intertidal sites from La Paz, Baja California Sur to northern
Oregon for benthic heterobranch sea slugs outside of their normal ranges. Combined
with records obtained from colleagues and internet sources, we document northern
range shifts for 37 species, including 21 (Berthella strongi, Okenia angelensis, Acan-
thodoris rhodoceras, Crimora coneja, Limacia mcdonaldi, Polycera atra, Triopha mac-
ulata, Carminodoris bramale, Doris cf. pickensi, Thordisa rubescens, Cadlina sparsa,
Doriopsilla albopunctata, Doriopsilla fulva, Doriopsilla gemela, Tritonia myrakeenae,
Doto lancei, Doto form A of Goddard (1996), Flabellina bertschi, Hermosita hakuna-
matata, Noumeaella rubrofasciata, Phidiana hiltoni) from new northernmost locali-
ties. The average range extension of these 21, plus Hermissenda opalescens and
Dirona picta reported by Merlo et al. (2018) from the west coast of Vancouver Island
was 270 km (SD = 201 km, n = 23). Significantly, no species were observed south of
their usual ranges during the 2014–17 marine heat wave. Combined with the results
of Goddard et al. (2016) for the 2014 warm anomaly, the 2014-17 marine heat wave
in the Northeast Pacific drove range shifts in at least 52 species of benthic hetero-
branchs, approximately one quarter of the species known from the region. These
numbers appear to be unprecedented in the historical record and point to global
warming as a contributing factor, likely acting through a series of steps leading to
increased poleward transport of coastal waters in the region, as well as elevated sea-
surface temperatures.
KEYWORDS: Range shifts, heterobranch sea slugs, nudibranchs, Northeast Pacific Ocean,
marine heat wave, El Niño, global warming
107
INTRODUCTION
The 2015-16 El Niño in the tropical Pacific was one of the strongest on record. However, its
physical effects on the California Current System, including coastal waters, were weaker than
expected (Jacox et al. 2016). This resulted in part because as the El Niño formed, the entire north-
east Pacific was already in the midst of a multi-year marine heat wave of unprecedented magnitude
(Bond et al. 2015; Di Lorenzo and Mantua 2016), causing extensive biological impacts at all troph-
ic levels and poleward range shifts typically observed only during strong El Niño events (reviewed
by Cavole et al. 2016; and see Jones et al. 2018). The range shifts driven by the 2014-15 warm
anomaly included 30 species of heterobranch sea slugs (heterobranchs), nine of which were found
in new northernmost localities (Goddard et al. 2016). During the 2015-16 El Niño, Merlo et al.
(2018) found Hermissenda opalescens, which was separated by Lindsay and Valdés (2016) from
its more northerly pseudocryptic sister H. crassicornis, on the west coast of Vancouver Island,
British Columbia. Merlo et al. (2018) also reported Dirona picta for the first time north of Oregon.
Here, we document additional range extensions of northeast Pacific heterobranchs associated with
the 2015-16 El Niño and the warm water anomaly that persisted into 2017 in the northern Califor-
nia Current System (Well et al. 2017) and summarize the effects of the combined warm water
events (hereafter the 2014-17 marine heat wave) on the distribution of heterobranchs in the region.
METHODS AND STUDY SITES
From fall 2015 through 2017, we sampled for benthic heterobranchs at mostly intertidal sites
from Baja California Sur, Mexico to Oregon (Table 1), including many of the same sites sampled
annually to quarterly by Goddard et al. (2016) using timed counts. We photographed living speci-
mens in the field or laboratory. A few were collected and deposited in the Invertebrate Zoology
Collection at the California Academy of Science (CAS) as voucher specimens and are referenced
below by their CASIZ catalog numbers, records of which can be accessed online via the CAS
Invertebrate Zoology Collection Database <http://researcharchive.calacademy.org/research/izg/
iz_coll_db/index.asp>. We were also sent new records of occurrence by colleagues, particularly in
Washington and British Columbia, and we also monitored citizen science posts on websites such
as iNaturalist, OCDiving, and Flickr for sightings of heterobranchs beyond their usual ranges.
From both of these latter types of sources we include below only records accompanied by an image
and the date and locality of observation.
We calculated the range shift for each species by using the Ruler tool on Google Earth to meas-
ure the straight-line distance between the previous northernmost known locality and its new north-
ernmost locality documented below. This measure is conservative and actually measures range
extensions, because it is based on the distance between recorded northernmost localities, typically
reached during strong El Niño events, rather than the distance between the new northernmost local-
ity and a species’ usual northern range limit. However, information on the latter has not actually
been compiled, and is spotty, scattered throughout a wide range of sources, and for many species
qualitative in nature.
Nomenclature used below follows the World Register of Marine Species (WoRMS)
<http://www.marinespecies.org/index.php>, as of June 2018.
RESULTS
Including Hermissenda opalescens and Dirona picta, whose ranges were extended by Merlo
et al. (2018), 23 species of heterobranchs were recorded from new northernmost localities from late
108 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES
Series 4, Volume 65, 28 Sept. 2018, No. 3
GODDARD ET AL.: EL NIÑO IMPACT ON HETEROBRANCH SEA SLUG RANGES 109
Site Latitude, Longitude
Bear Cove, Port Hardy, Vancouver Is., BC, Canada (subtidal) 50.7222° -127.4597°
Monas Is., Lemmens Inlet, Clayoquot Sound, Vancouver Is., BC (oyster racks) 49.1904° -124.8859°
East end of Stockham Island, Clayoquot Sound, Vancouver Is., BC (kelp bed) 49.1692° -125.8937°
Chibahdehl Rocks, Cape Flattery, WA (subtidal) 48.3942° -124.6774°
Haystack Rock, Cannon Beach, OR 45.8844° -123.9670°
Oceanside Beach State Park, OR 45.4619° -123.9729°
Netarts Bay, OR (subtidal) 45.4301° -123.9456°
South side Netarts jetty, Netarts Bay, OR 45.4293° -123.9476°
South side of Boiler Bay, OR 44.8289° -124.0634°
Otter Crest, OR 44.7529° -124.0656°
Yaquina Bay, OR 44.6246° -124.0433°
Seal Rock State Wayside, OR 44.4918° -124.0861°
Yachats, OR 44.3138° -124.1095°
Neptune State Scenic Viewpoint, OR 44.2634° -124.1101°
Strawberry Hill, OR 44.2509° -124.1143°
Bob Creek, OR 44.2423° -124.1127°
Gregory Point, OR 43.3400° -124.3749°
Cape Arago, OR
North Cove 43.3094° -124.3986°
Middle Cove 43.3026° -124.4007°
South Cove 43.3026° -124.3988°
Crook Point, OR 42.2511° -124.4136°
Whiskey Creek, OR 42.2227° -124.3830°
House Rock, OR 42.1130° -124.3550°
Lone Ranch, OR 42.0997° -124.3493°
Palmer’s Point, CA 41.1319° -124.1642°
Woodley Island, Humboldt Bay, CA 40.8077° -124.1666°
MacKerricker State Park, CA 39.4907° -123.8035°
Glass Beach, CA 39.4533° -123.8143°
Moat Creek, CA 38.8794° -123.6809°
Salt Point State Park, CA 38.5648° -123.3332°
Coleman Beach, CA 38.3632° -123.0708°
Miwok Beach, CA 38.3612° -123.0701°
Pinnacle Rock, CA 38.3050° -123.0172°
Dillon Beach, CA 38.2538° -122.9695°
Drake’s Estero, CA 38.0351° -122.9279°
Duxbury Reef, CA 37.8903° -122.6998°
Elkhorn Slough, CA 36.8090° -121.7849°
Monterey Breakwater, CA (subtidal) 36.6085° -121.8905°
Carmel Point, CA 36.5435° -121.9342°
Point Sierra Nevada, CA 35.7130° -121.3167°
Estero Bluffs State Park, CA 35.4464° -120.9440°
T pier, Morro Bay, CA (subtidal) 35.3694° -120.8559°
Morro Bay, CA 35.3440° -120.8448°
Hazard Canyon Reef, CA 35.2897° -120.8844°
Point Buchon, CA 35.2551° -120.8996°
Cave Landing, CA 35.1752° -120.7223°
Tarantula Reef, CA 34.4952° -120.4972°
Gaviota, CA 34.4686° -120.2373°
Naples, CA 34.4337° -119.9501°
Ellwood Mesa Reef, CA (subtidal) 34.4177° -119.9015°
Northeast Santa Cruz Island, CA (subtidal) 34.0449° -119.6015°
Anacapa Island, CA (subtidal)
N side, East Anacapa Is. 34.0175° -119.3667°
Pelican Preserve, West Anacapa Is. 34.0121° -119.4157°
S side, West Anacapa Is. 34.0079° -119.4381°
Dana Point Harbor, California (docks) 33.4605° -117.7069°
Mission Bay, San Diego, CA (subtidal) 32.7617° -117.2466°
Punta Entrada, Isla Magdalena, Bahía de Magdalena, BCS (subtidal) 24.5443° -112.0588°
Playa Pichilingue, La Paz, BCS 24.2854° -110.3283°
TABLE 1. Names and geographic coordinates of recent collecting sites from British Columbia (BC, Canada),
Washington (WA), Oregon (OR), California (CA), and Baja California Sur (BCS). All sites intertidal unless noted
otherwise.
2015 through 2017 and are listed systematically in Section 1 below. For each of these we include
their known southern range limit and previous northern range limit, along with the primary refer-
ences documenting those. We also include, as “additional northern localities,” records from sites
located between the new and previous northernmost localities; for a few species these also include
older, previously undocumented or obscure records.
New northernmost sites were spread over 26 degrees of latitude, from La Paz, Baja California
Sur (for Carminodoris bramale) to Port Hardy, Vancouver Island, British Columbia (for Triopha
maculata). Range extensions varied in length from 23 to 700 km, with a mean of 270 km (SD =
201 km, n = 23).
Section 2 covers species found at or near previously determined northern range limits.
Each of the recent collecting localities mentioned below is listed with its geographic coordi-
nates in Table 1.
I. New northernmost locality records
Heterobranchia
Pleurobranchida
Berthella strongi (MacFarland, 1966). MacKerricker State Park, Mendocino Co., California,
1 specimen, low rocky intertidal, 4 July 2016 (Pirrone 2016) to El Tomatal, Baja California,
Mexico (Goddard and Green 2013; for image see <https://www.inaturalist.org/
observations/2957040>).
Previous northernmost locality: Moss Beach, California (Bertsch et al. 1972 [as Pleuro-
branchus strongi]).
Additional northern localities: Salt Point State Park, Sonoma Co., California, 1 specimen, low
intertidal, 9 May 2016 (observed by WP, DM, PD); Drake’s Estero, Point Reyes National Park,
Marin Co., California, 1 specimen, with an egg mass, next to its sponge prey Oscarella carmela,
under a low intertidal cobble, 8 June 2016 (observed by JG).
Remarks: Behrens (1998, 2004) reported B. strongi found by Mike Miller off of Nanaimo,
British Columbia. No collection information, including date, or image were given, but M. Miller
(personal communication to JG, 9 July 2016) dove there in 1998, and the record therefore may rep-
resent an ephemeral range extension driven by the strong 1997-98 El Niño event. However, it
should be noted that this species has not been reported from north of California before or since, and
without an image or specific collection data we consider this record unverified.
Nudibranchia
Goniodorididae
Okenia angelensis Lance, 1966. Miwok Beach, Sonoma Co., California, 1 specimen, 5 mm
long, low rocky intertidal, 27 May 2017, observed by Colby Davidson (Fig. 1A) (Hollis Bewley,
personal communication to JS, 5 June 2017) to Punta Rosarito, Baja California, Mexico (Goddard
and Hermosillo 2008); Bahía de los Ángeles, Baja California (Lance 1966) and Chile (Muñoz et
al. 1996; Schrödl 1996).
Previous northernmost locality: San Francisco Bay, California (Lance 1966).
Remarks: The new record is also significant for its location on the outer coast, outside the sea-
sonal warm water refugium of San Francisco Bay.
110 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES
Series 4, Volume 65, 28 Sept. 2018, No. 3
Onchidorididae
Acanthodoris rhodoceras Cockerell in Cockerell and Eliot, 1905. Chup Point, Barkley Sound,
Vancouver Island, British Columbia, 1 specimen, 12 m depth, 21 May 2018 (Fig. 1B) found by
Kathy Johnson (P. Mieras, personal communication to JG, 2 June 2018) to Bahía Tortugas, Baja
California, Mexico (Behrens 1991) and Bahía de los Ángeles, Baja California (Bertsch 2014).
Previous northernmost locality: South side of Netarts Jetty in Netarts Bay, Oregon, 1 specimen
12 mm long, low intertidal, 17 June 2015 (observed by TP; see Maginnis 2016).
Remarks: The identity of specimens collected in the 1960s from Alaska (including the Arctic
Ocean) and Vancouver Island by J. McLean, and referred to as A. rhodoceras by Fahey and Valdés
(2005), needs to be verified for the following reasons. First, except for the specimen recently found
in Barkley Sound, there are no other records of A. rhodoceras from north of Oregon, including
from Bernard (1970), Millen (1983, 1989), Lee and Foster (1985), Goddard et al. (1997), Goddard
and Foster (2002), Lamb and Hanby (2005), and Fletcher (2013). Second, no other heterobranch
gastropod is known to have a geographic distribution extending from the Arctic Ocean into the
Gulf of California (see Behrens and Hermosillo 2005), especially as recent integrative systematic
studies have shown that nudibranchs from the Northeast Pacific Ocean once considered to have
broad geographic ranges are actually complexes of species with more limited, but overlapping
ranges (e.g., Lindsay et al. 2016; Lindsay and Valdés 2016). Based on the records of A. pilosa
(Abildgaard, 1789) and the closely related A. atrogriseata O’Donoghue, 1927 from the North
Pacific, including the Aleutian Islands and south central Alaska (Lee and Foster 1985; Hallas et al.
2016), we think it likely the specimens collected by McLean in Alaska are either one or both of
those species, a result likely to influence the biogeographic analyses conducted by Hallas et al.
(2016), who relied on the distribution information given by Fahey and Valdés (2005) for
A. rhodoceras, and who incorrectly showed it in their Figure 3 as being the only species of Acan-
thodoris present along most of the Pacific coast of Alaska.
Polyceridae
Crimora coneja Er. Marcus, 1961. Boiler Bay, Lincoln Co., Oregon, 29 April 2017, 2 speci-
mens, low rocky intertidal at south end of bay, observed by Lillian Mayer and her Biology class
from Clackamas Community College (L. Mayer, personal communication to JG, 1 May 2017; for
image see Nosler 2017) to Point Loma, San Diego, California (Marcus 1961).
Previous northernmost locality: North Cove, Cape Arago, Oregon (Goddard 1984).
Limacia mcdonaldi Uribe, Sepúlveda, Goddard and Valdés, 2017. Moat Creek Beach, Men-
docino Co., California, 24 June 2017, 1 specimen, low rocky intertidal (observed by JG; for image
see <https://www.inaturalist.org/observations/6868719>) to Cabo San Lucas (Lance 1961) and
into the Gulf of California to Bahía de los Ángeles (Keen 1971; Angulo-Campillo 2003, 2005).
Previous northernmost locality: Not clear, owing to identification until 2017 as L. cockerelli
(MacFarland, 1905). Images show that L. mcdonaldi has occurred on the Monterey Peninsula since
at least the 1960s and 70s (e.g., McDonald 2016; Goddard 2017a). Since 2014 L. mcdonaldi has
also been recorded many times from San Mateo and Marin counties (RA, personal observations;
and see <https://www.inaturalist.org/observations?verifiable=true&taxon_id=538831&place_id=
&preferred_place_id=&locale=en>).
Additional northern localities: Salt Point State Park, Sonoma Co., California, 9 May 2016,
1 specimen, low rocky intertidal (observed by WP, DM, PD). Drake’s Estero, Point Reyes Nation-
al Seashore, California, 15 specimens, low rocky intertidal shelf just inside mouth of the estero,
8 June 2016 (observed by JG; for image see <https://www.inaturalist.org/observations/5397011>).
GODDARD ET AL.: EL NIÑO IMPACT ON HETEROBRANCH SEA SLUG RANGES 111
Polycera atra MacFarland, 1905. Monas Island, Lemmens Inlet, Meares Island, Clayoquot
Sound, Vancouver Island, British Columbia, several specimens on suspended oyster culture array
next to Monas Island, July and August 2015 (Fig. 1C) (A. Murray, personal communication to JG,
26 April 2017) to Punta Pericos, Baja California Sur (Angulo-Campillo 2003, 2005).
Previous northernmost locality: Westport, Grays Harbor, Washington (Lamb and Hanby 2005;
and see Goddard et al. 2016).
Additional localities in Oregon: Seal Rock, 8 May 2016, 1 specimen (observed by TP);
Neptune State Scenic Viewpoint, 20 May 2015, 1 specimen (TP); Strawberry Hill, 8 April 2016,
1 specimen (TP).
Triopha maculata MacFarland, 1905. Bear Cove, Port Hardy, Vancouver Island, British
Columbia, 19 total specimens, with 7 egg masses, 3-12 m depth, September to October 2015,
observed and photographed by Jackie Hildering, plus 1 specimen, 4 m depth, 22 October 2016,
observed and photographed by Alexandra Spicer (records listed by Pacific Northwest Shell Club
2016) to Punta Rosarito, Baja California (Goddard and Schickel 2000).
Previous northernmost locality: Bamfield, Vancouver Island, British Columbia (Millen 1983).
Additional northern localities: Entrance of Lemmens Inlet, Clayoquot Sound, Vancouver
Island, British Columbia, many specimens with egg masses on Macrocystis pyrifera adjacent to the
east end of Stockham Island, August - October 2015 (A. Murray, personal communication, with
images, to JG, 22 March 2016).
Remarks: Jackie Hildering, an experienced underwater naturalist and observer of nudibranchs,
reported (personal communication to JG, 16 March 2016) that in approximately 150 dives over 15
years in the Port Hardy area, she had not observed T. maculata before September 2015.
Discodorididae
Carminodoris bramale (Fahey and Gosliner, 2003). Playa Pichilingue, La Paz, Baja Califor-
nia Sur, Mexico, 12 specimens, up to 75 mm long, with egg ribbons, on and near encrusting
yellow sponge on the underside of low intertidal cobbles in the outlet of the lagoon behind the
playa, 27 December 2017 (observed by JG; for images see: <https://www.inaturalist.org/observa
tions/9332510>) to Isla de Coiba, Panama (Hermosillo 2004 [as Hoplodoris bramale]).
Previous northernmost locality: La Cruz de Huanacaxtle, Bahía de Banderas, Mexico (Her-
mosillo 2006).
Remarks: The specimens from La Paz are the first record of C. bramale from the Gulf of Cal-
ifornia and the Baja California peninsula. It was not recorded by Angulo-Campillo (2005) during
his four year survey of opisthobranchs from Baja California Sur, including the La Paz area.
Thordisa rubescens Behrens and Henderson, 1981. Northeast Santa Cruz Island, California,
1 specimen, 15 m depth, 1 November 2017 (Figure 1D), observed by David Kushner, Kenan Chan,
and Joshua Sprague (D. Kushner, personal communication to JG, 13 November 2017) to Punta
Eugenia, Baja California Sur (Bertsch et al. 2000).
Previous northernmost locality: Paradise Cove, Malibu, Los Angeles Co., California (Behrens
and Henderson, 1981).
Remarks: The specimen from Santa Cruz Island appeared to be dull orange to rust colored, but
had the distinctive “halos” of lighter pigment around the rhinophores and gill plume described by
Behrens and Henderson (1981) for this species (Figure 1D).
Few specimens of this Californian species have been found since its original description
(Behrens 2016), so it is noteworthy that “dozens” have been observed, including some mating and
112 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES
Series 4, Volume 65, 28 Sept. 2018, No. 3
laying eggs, the past two years on subtidal reefs around the Palos Verdes Peninsula (P. Garner, per-
sonal communication to RA, 20 June 2018; and see <https://www.inaturalist.org/taxa/50139
-Thordisa-rubescens>).
Although Behrens and Henderson (1981) reported finding one specimen off the Palos Verdes
Peninsula, the other three specimens they listed all came from “Big Kelp Reef, Paradise Cove, Los
Angeles Co.,” and the geographic coordinates they gave for that site place it in Malibu, not Palos
Verdes as implied in Behrens and Hermosillo (2005).
GODDARD ET AL.: EL NIÑO IMPACT ON HETEROBRANCH SEA SLUG RANGES 113
FIGURE 1. Heterobranch sea slugs found at new northernmost localities in the Northeastern Pacific Ocean, 2015–2017.
A Okenia angelensis, Miwok Beach, Sonoma Co., California, 27 May 2017. Image by Colby Davidson. B Acanthodoris
rhodoceras, Chup Point, Barkley Sound, Vancouver Island, British Columbia, 21 May 2018. Image by Peter Mieras/subvi-
sionproductions.com. C Polycera atra, Lemmens Inlet, Clayoquot Sound, Vancouver Island, British Columbia, 25 July
2015. Inset: tail. Images by Brandon Exner. D Thordisa rubescens, Santa Cruz Island, California, 1 November 2017. Image
by Kenan Chan/Channel Islands National Park.
Dorididae
Doris cf. pickensi Ev. Marcus and Er. Marcus, 1967. Morro Bay, San Luis Obispo Co., Cali-
fornia, 7 specimens, on encrusting yellow sponge, 4 m depth near T Pier, 25 May 2016 (Fig. 2A)
(observed by CH) to La Jolla, California (observed by JG, CASIZ 186472); northern Gulf of Cal-
ifornia (Marcus and Marcus 1967) to Costa Rica (Camacho-García et al. 2005).
Previous northernmost locality: Naples, Santa Barbara Co., California (Goddard and Green
2013; Goddard 2017).
Remarks: A specimen found by CH in Morro Bay laid a flat egg ribbon identical to that
described by Goddard and Green (2013, p. 57) for this species from Santa Barbara County.
With their uniform yellow coloration and lack of dark pigmentation, up to 15 unipinnate gills,
low rounded spiculate dorsal papillae, triangular labial tentacles, and hamate radular teeth (for
images see Goddard 2017b), specimens of this species from California differ from all other yellow
dorid nudibranchs known from the Northeast Pacific Ocean and may be undescribed. They are
closest to Doris pickensi originally described by Marcus and Marcus (1967) and redescribed by
Camacho-García and Gosliner (2008), but need to be fully compared – including with molecular
genetics – with specimens from the vicinity of the type locality of that species at Puerto Peñasco
in the northern Gulf of California to resolve their identity.
Cadlinidae
Cadlina sparsa (Odhner, 1921) Drakes’ Estero, Point Reyes National Seashore, California,
3 specimens, low rocky intertidal, 8 June 2016 (observed by JG; for image see <http://www.
inaturalist.org/observations/5855244>) to Punta Rosarito, Baja California, Mexico (JG, personal
observations, 28 May 2001); Bahía de Banderas to Panama (Hermosillo 2004, Table 2; Hermosil-
lo et al. 2006); Chile and Argentina (Marcus 1959; Schrödl 2000).
Previous northernmost locality: Marin Co. headlands, California (Jaeckle 1983).
Additional northern localities: Duxbury Reef, California, 1 specimen, 21 December 1992
(CASIZ 66769), 1 specimen, 23 December 2011 (JG, personal observations).
Dendrodorididae
Doriopsilla albopunctata (Cooper, 1863). Whiskey Creek, Curry Co., Oregon, 1 specimen,
low rocky intertidal, 29 May 2017 (Fig. 2B) (observed by NT) to San Diego, California and
possibly Baja California (Hoover et al. 2015).
Previous northernmost locality: not clear, owing to inclusion of D. fulva as a junior synonym
of D. albopunctata until publication of Hoover et al. (2015). The latter authors give Mendocino,
California as the northern range limit of D. albopunctata.
Additional northern localities: Palmer’s Point, Patrick’s Point State Park, California, 2 speci-
mens, low rocky intertidal, 7 June 2016 (observed by JG). Glass Beach, Fort Bragg, California,
1 specimen, low rocky intertidal, 23 June 2017 (observed by JG; for image see <https://www.
inaturalist.org/observations/6872674>).
Doriopsilla fulva (MacFarland, 1905). Netarts Bay, Oregon, at least 14 total specimens, rock
rubble, 4–8 m depth, April, June, July, August 2016, June 2017 (Fig 2C) (Todd Cliff, personal com-
munications to JG, 18 December 2016 and 25 June 2017) to Laguna Guerrero Negro, Baja Cali-
fornia, Mexico (Bertsch and Aguilar Rosas 2016).
Previous northernmost locality: Whiskey Creek, Curry Co., Oregon (Goddard et al. 2016).
Additional northern localities: Middle Cove, Cape Arago, Oregon, low rocky intertidal, 3 spec-
114 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES
Series 4, Volume 65, 28 Sept. 2018, No. 3
imens (CASIZ 216866, 209506, 209501), 5 June 2016 (observed by JG and NT; for image see
<http://www.inaturalist.org/observations/3528069>); 1 specimen, 27 May 2017 (observed by NT).
Crook Point, Curry Co., Oregon, 2 specimens, low rocky intertidal, 7 February 2016 (observed by
NT).
Remarks: Goddard et al. (2016) reported finding a single juvenile D. fulva at Whiskey Creek,
Oregon in June 2015, the first specimen of this species reported from north of California. One year
later (6 June 2016) at the same site JG and NT counted 43 specimens of D. fulva, and a year after
that (29 May 2017) NT found 11 specimens. For the southern Oregon coast as a whole, only two
specimens of D. fulva were found in 2015 (Goddard et al. 2016). This was based on 37 trips to 20
sites, largely by NT. The following year NT counted a total of 204 individuals in 19 visits to 13 of
those same sites, finding D. fulva at seven of them. Through the first half of 2017 NT had counted
24 total individuals of D. fulva at four out of 10 sites visited in southern Oregon. Todd Cliff and
Andy Lamb found at least 5 specimens in Netarts Bay on 5 June 2017 (Todd Cliff, personal com-
munication to JG, 25 June 2017).
Doriopsilla gemela Gosliner, Schaefer and Millen, 1999. Elkhorn Slough, Moss Landing,
California, 1 specimen, 4 m depth, just inside entrance to slough, 5 July 2016 (Bentall 2016) to
Bahía Tortugas, Baja California Sur (Bertsch and Aguilar Rosas (2016).
Previous northernmost locality: Monterey, California (Hoover et al. 2015; Goddard et al.
2016; and see <https://www.inaturalist.org/observations/5220737>).
Additional northern localities: T Pier, Morro Bay, California, 19 specimens with egg masses
on shell rubble, 3–4 m depth, 25 May 2016 (observed by CH).
Tritonidae
Tritonia myrakeenae Bertsch and Mozqueira, 1986. Estero Bluffs State Park, San Luis Obis-
po Co., California, 3 specimens, among the octocoral Clavularia sp. under low intertidal cobbles,
29 April 2017 (observed by JG; for image see <https://www.inaturalist.org/observa-
tions/6358562>) to Costa Rica and Panama (Camacho-García et al. 2005).
Previous northernmost locality: Santa Barbara, California (Behrens 1980).
Additional northern localities: Cave Landing, San Luis Obispo Co., 4 specimens, 27 May
2013; 1 specimen, 8 October 2014; 1 specimen, 9 March 2016 (observed by JG); Tarantula Reef,
Jalama Beach, Santa Barbara Co., 1 specimen, 5 July 2012; 1 specimen, 2 February 2015 (observed
by JG); Gaviota, Santa Barbara Co., 6 specimens, 7 May 2012 (observed by JG); Naples, Santa
Barbara Co., 1186 specimens, October 2006 – April 2017 (observed by JG).
Remarks: This diminutive tritonid, which has been by far the most abundant nudibranch at
Naples, is usually found associated with the stoloniferous octocoral Clavularia sp., on whose
polyps it preys (for image see <https://www.inaturalist.org/observations/5396758>).
Dotoidae
Doto lancei Ev. Marcus and Er. Marcus, 1967. Dana Point Harbor, California, 1 specimen,
18 November 2017 (Stacey 2017) to Panama (Hermosillo 2004).
Previous northernmost locality: Mission Bay, San Diego, California (Behrens 1991).
Remarks: Behrens (2004) reported D. lancei from Monterey Bay, but without an image to
confirm the identification, we suspect it was actually D. columbiana O’Donoghue, 1921, which is
common in central and northern California and superficially resembles light colored D. lancei but
has shorter ceratal tubercles lacking the apical spots characteristic of D. lancei.
GODDARD ET AL.: EL NIÑO IMPACT ON HETEROBRANCH SEA SLUG RANGES 115
Doto form A of Goddard (1996). Woodley Island, Humboldt Bay, Humboldt Co., California,
1 specimen on side of floating dock, 20 May 2016 (Young 2016) to Punta Rosarito, Baja Califor-
nia (JG, personal observations) and probably Baja California Sur (Angulo-Campillo 2005
[as D. amyra]).
Previous northernmost locality: Drake’s Estero, Point Reyes National Seashore (Goddard
1996).
Additional northern localities: Coleman Beach, Sonoma Co., California, 2 specimens, low
rocky intertidal, 26 June 2017 (observed by JG; for image see <https://www.inaturalist.org/
observations/6847120>).
Remarks: This form is often identified as Doto amyra, but differs from that species in mor-
phology, egg size, mode of development, and genetics (see Goddard et al. 2016, p. 29).
Dironidae
Dirona picta MacFarland in Cockerell and Eliot, 1905. Barkley Sound, Vancouver Island,
British Columbia, at least 1 specimen, summer 2016 (Merlo et al. 2018; C. Tamis, personal
communication to JG, with images, 12 June 2018) to Baja California Sur, and northern Gulf of
California (Farmer and Collier 1963; and see CASIZ Collection database).
Previous northernmost locality: Cape Meares, Oregon (Goddard 1997).
Additional northern localities: Seal Rock State Wayside, Oregon, low rocky intertidal, 2 total
specimens, 7 June and 3 July 2016 (observed by TP).
Flabellinidae
Flabellina bertschi Gosliner and Kuzirian, 1990. Anacapa Island, California, 1 specimen, 12
m depth, South side of West Anacapa Is., 26 Aug 2016 (Klug 2016a) to Panama (Hermosillo 2004).
Previous northernmost locality: Big Fisherman’s Cove, Santa Catalina Island (Goddard et al.
2016).
Additional northern localities: Mission Bay Point, San Diego, California, 1 specimen, 2 m
depth, rock rubble, 20 May 2016 (observed by CH). Mission Bay Drive bridge, San Diego, Cali-
fornia, at least 24 specimens on pier pilings, maximum depth 5 m, 21 November 2016 (observed
by BG; for image see <https://www.inaturalist.org/observations/4632067>).
Facelinidae
Hermissenda opalescens (Cooper, 1863). Yellow Bank, Clayoquot Sound, Vancouver Island,
British Columbia, 24 specimens, 15 July 2016 (Merlo et al. 2018) to Baja California Sur (Angulo-
Campillo 2005); northern Gulf of California, Mexico (Farmer and Collier, 1963; Keen 1971).
Previous northernmost locality: Charleston, Oregon (Goddard 1984 [as H. crassicornis, form
lacking bluish-white stripe on cerata; see remarks below])
Additional northern localities: 7 localities in Barkley Sound, Vancouver Island, British Colum-
bia, summer 2016 (Merlo et al. 2018), Cape Flattery, Washington (Chibahdehl Rocks, Box Canyon,
Steve’s Cave), August 2015 (Fig. 2D) (K. Fletcher, personal communication with images to JG, 26
April 2016), Haystack Rock, Cannon Beach (Cullin 2017), Oceanside Beach State Park (observed
by TP, 24 April 2016), Otter Crest (observed by TP, June to July 2016), Seal Rock (observed by TP,
May to July 2016), Strawberry Hill (observed by TP, April to July 2016 and JG, 4 June 2016; for
image see <http://www.inaturalist.org/observations/3527960>), Bob Creek (observed by TP,
7 May and 5 July 2016). Additional records of H. opalescens from Oregon in 2016 and 2017 are
available on iNaturalist (<http://www.inaturalist.org/taxa/494603-Hermissenda-opalescens>).
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Remarks: Lindsay and Valdés (2016) reinstated H. opalescens as distinct from H. crassicornis
(Eschscholtz, 1831) and showed that externally H. opalescens can be distinguished in the North-
east Pacific Ocean from H. crassicornis by the lack of white stripes on the cerata of the former.
The two color forms have long been recognized in field guides to nudibranchs from the northeast-
ern Pacific Ocean (e.g., Behrens 1980; McDonald and Nybakken 1980). Lindsay and Valdés (2016,
pp. 7 and 8) described the range of H. opalescens as extending from “the Sea of Cortez through
Oregon,” but in their conclusions described H. opalescens as ranging north only to Bodega Bay,
apparently using a more conservative standard based solely on specimens they sequenced. They
then stated that H. crassicornis and H. opalescens overlap in range “between Point Reyes and
GODDARD ET AL.: EL NIÑO IMPACT ON HETEROBRANCH SEA SLUG RANGES 117
FIGURE 2. Nudibranch sea slugs found at new northern localities in the Northeastern Pacific Ocean, 2015–2017.
A Doris cf. pickensi, Morro Bay, California, 25 May 2016. Image by CH. B Doriopsilla albopunctata, Whiskey Creek,
Curry Co., Oregon, 19 May 2017. Image by NT. C Doriopsilla fulva, Netarts Bay, Oregon, 16 July 2016. Image by Todd
Cliff. D Hermissenda opalescens, Box Canyon, Neah Bay, Washington, 20 August 2015. Image by Doug Miller.
Bodega Bay,” a distance of only a few km. However, based on the presence or absence of the
ceratal stripes, images by Bruce Wight available on the Sea Slug Forum <http://www.seaslugforum.
net/showall/hermcras> show that H. crassicornis has been known since at least 2000 from as far
south as San Miguel Island, California. Further, Goddard (1984, 1987, 1990), citing Behrens
(1980), noted directly or indirectly the presence of non-striped Hermissenda (what we now know
to be H. opalescens) at Charleston, Cape Arago, and Humbug Mountain, Oregon, and Punta Gorda
in northern California. He found few H. opalescens relative to the numbers of H. crassicornis at
these sites, and their occurrence was probably associated with the El Niño events of 1982-83 and
1986-88 (for images see <https://www.inaturalist.org/observations/12907271>, <https://www.
inaturalist.org/observations/12771009>). Hermissenda opalescens has therefore ranged to at least
southern Oregon in the past, and H. crassicornis to at least the edge of the Southern California
Bight, both likely as ephemeral range shifts driven by opposite phases of the El Niño Southern
Oscillation (ENSO).
Hermosita hakunamatata (Ortea, Caballer and Espinosa, 2003). Punta Entrada, Isla Mag-
dalena, Bahía Magdalena, Baja California Sur, Mexico, 3 specimens, with egg masses, on hydroid
Solanderia, 2-5 m depth, 1 September 2015 (Fig. 3A) (observed by CH; also see Bertsch and
Aguilar Rosas 2016) to Panama (Hermosillo 2004 [as Phestilla hakunamatata]).
Previous northernmost locality: Isla Isabella, Nayarit, Mexico (Hermosillo 2004).
Remarks: The specimens from Bahía Magdelena are the first record of H. hakunamatata from
the Baja California peninsula. It was not recorded by Angulo-Campillo (2005) during his four year
survey of opisthobranchs from Baja California Sur, including Bahía Magdelena.
Noumeaella rubrofasciata Gosliner, 1991. Outer Pinnacles, Carmel Bay, California, 1 speci-
men, 43 m depth, 4 March 2017 (C. Bauder, personal communication to JG, 5 March 2017; Baud-
er 2017) to Panama (Hermosillo 2004).
Previous northernmost locality: Malibu, California (Goddard et al. 2016).
Additional northern localities: Anacapa Island, California, 1 specimen, 12 m depth, north side
of East Anacapa Is., 10 February 2018 (Klug 2018).
Phidiana hiltoni (O’Donoghue, 1927). Pinnacle Rock, Bodega Bay, Sonoma Co., California,
7 specimens, low rocky intertidal, 25 November 2015 (Sones 2015) to Cedros Island, Baja Cali-
fornia, Mexico (Farmer and Collier 1963).
Previous northernmost locality: Palomarin, Marin Co., California (WP and DM, personal
observations, January 2011); Duxbury Reef (Behrens 2004; and see Goddard et al. 2011).
Additional northern localities: Dillon Beach, Marin Co., California, low rocky intertidal, April
2014 – December 2017 (Thompson, 2017), and 8 specimens, 30 April 2017 (Fig. 3B) (observed by
WP, DM, PD).
Remarks: P. hiltoni was first sighted in Bodega Bay at Pinnacle Rock in 2015, and 5 individ-
uals were recorded during a survey on 4 December 2017 (JS and ES, personal observations).
Thompson (2017) also recorded specimens from Dillon Beach, just 7 km south, in May, June, July,
and December 2016, as well as in March, May, July, and August 2017, also indicating the persist-
ence of this species in Bodega Bay following the initial sighting reported in 2015. Goddard et al.
(2011, Appendix) compiled historical records of heterobranchs from Marin and Sonoma counties,
which provide robust evidence for the historical absence of P. hiltoni in the region. Additional sig-
nificant records can be extracted from Steinberg (1963) and Marcus (1961), with many of those
records originating from the old Pacific Marine Station at Dillon Beach. Together, all of these
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sources document the occurrence from the 1940s through 1970s of nearly 50 species of hetero-
branchs from the outer coast of northern Marin and Sonoma counties, and Phidiana hiltoni is not
among them.
II. Additional species, at or near previous northernmost localities
In addition to the species listed above, 24 more were found in 2016 or 2017 at or near
previously determined northernmost range limits. Four of these (Aplysia californica, Aplysia
vaccaria, Flabellina cooperi, and Flabellinopsis iodinea) were found farther north in 2015–17 than
in 2014–15 as reported by Goddard et al. (2016), and are documented individually below, along
GODDARD ET AL.: EL NIÑO IMPACT ON HETEROBRANCH SEA SLUG RANGES 119
Figure 3. Nudibranch sea slugs found at new northern localities in the Northeastern Pacific Ocean, 2015–2017. A Her-
mosita hakunamatata, La Bocana, Bahía de Magdalena, Baja California Sur, Mexico, 1 September 2015. Image by CH. B
Phidiana hiltoni, Dillon Beach, California, 30 April 2017. Image by DM. C Taringa aivica, Mission Bay, San Diego, Cal-
ifornia, 14 June 2018. Image by CH. D Diaphoreolis lagunae, Whiskey Creek, Curry Co., Oregon, 19 May 2017 (grid
squares 2 mm on a side). Image by NT.
with 10 more species not included in Goddard et al. (2016). The remaining 10 species are listed in
Table 2.
Bulla gouldiana (Pilsbry, 1893). Elkhorn Slough, 1 specimen, intertidal mud flats, 16 May
2018 (Imkitayama 2018b). Morro Bay, California, intertidal muddy sand flats, May through mid-
November 2017 (observed by JG; for image see <https://www.inaturalist.org/
observations/3127748>; Eaton 2016). On 13 November 2016 shells measured up to 50 mm long,
and one yellow egg string was found (see <https://www.inaturalist.org/observations/6223507>).
Bentall (2017) noted only large, empty shells at one site in Morro Bay in March 2017, but in
November 2017 JG observed numerous large specimens and their egg strings (see
<https://www.inaturalist.org/observations/8818733>).
Remarks: The published northern limit of B. gouldiana is Morro Bay (Roller and Long 1969;
Behrens and Hermosillo 2005). However, Bulla gouldiana was also recorded as uncommon on
Bodega tide flats in a list of marine invertebrates from Sonoma Co. compiled by Victor Chow in
2013 (see <http://bml.ucdavis.edu/bmr/invert_list.PDF>). Additionally, Moss Landing Marine
Laboratories (MLML) has in its Invertebrate Collection a preserved specimen (Catalogue No.
MO600) collected from mudflats near the mouth of Elkhorn Slough in Monterey Bay (see
<http://digital.mlml.calstate.edu/islandora/object/islandora%3A15334>). No collection date is
given, but the specimen was identified by John Cooper, who was a graduate student at MLML in
the 1970s. This specimen presumably forms the basis for the inclusion of B. gouldiana in species
lists for Elkhorn Slough available in technical reports (e.g., DeVogelaere et al. 1998).
At Naples, an open coast site on the south coast of Santa Barbara Co., B. gouldiana was absent
from 2006 until late 2015, reached high adult densities by winter 2016, laid egg strings in May and
June 2016, was absent by September 2016, and, in contrast to the population in Morro Bay, has not
been observed again through mid-2018 (Fig. 4).
Aplysia californica (Cooper, 1863). Yaquina Bay, Oregon, August 2016; one large specimen
was found in a water storage reservoir, filled from Yaquina Bay, used by the Oregon Coast Aquar-
ium (Pearsall 2016).
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Species Site(s) Source
Navanax inermis (Cooper, 1863) Bodega Harbor, Tomales Bay, Drake’s
Estero, CA iNaturalist
Okenia rosacea (MacFarland, 1905) Cape Arago, OR iNaturalist
Thordisa bimaculata Lance, 1966 Monterey Peninsula Observations by BG on iNaturalist
Felimare californiensis (Bergh, 1879) Anacapa & Santa Cruz Islands, CA “divindk” [D. Klug] on Flickr
Felimida macfarlandi (Cockerell, 1901) Monterey, CA Observations by BG, RA, & others on
iNaturalist
Janolus anulatus Camacho-García & Gosliner, 2006 Tarpits Reef, Carpinteria, CA Observations by JG on iNaturalist
Janolus barbarensis (Cooper, 1863) San Francisco Bay, CA iNaturalist
Anteaeolidiella oliviae (MacFarland, 1966) Sonoma coast, CA iNaturalist
Babakina festiva (Roller, 1972) Fitzgerald Marine Reserve, CA iNaturalist
Cuthona phoenix Gosliner, 1981 Monterey, CA Observations by RA on iNaturalist
TABLE 2. Species included in Goddard et al. (2016) that were found in 2016–17 at or near, but not beyond, previously
determined northern range limits. The relevant observation(s) can be found by searching by species the websites given in
the right column. Initials in the right column refer to authors of the present study.
Remarks: The specimen noted above was most likely pumped into the reservoir as a free-
swimming veliger larva. Aplysia californica has been reported from as far north as Yaquina Bay
once before, during the strong 1982-83 El Niño (Pearcy and Schoener 1987).
Aplysia vaccaria Winckler, 1955. Elkhorn Slough, Monterey Bay, California, at least 2 spec-
imens and egg strings, low rocky intertidal, 8 July 2016 (Blue Water Ventures 2016); at least 1
specimen, “low tide,” 16 May 2018 (Imkitayama 2018a).
Remarks: Behrens (1991) first reported Aplysia vaccaria from Monterey Bay but did not spec-
ify a precise locality. Therefore the above observations from Elkhorn Slough might represent a
small northward range extension from Monterey, where A. vaccaria was found in December 2014
(RA, personal observations, for image see <https://www.inaturalist.org/observations/1132630>),
September and October 2015 (Goddard et al. 2016; BG personal observations, for image see
<https://www.inaturalist.org/observations/5181629>).
Aplysia vaccaria is usually found south of the Palos Verdes Peninsula (JG, personal observa-
tions). At Naples, Santa Barbara Co., it appeared briefly in late 2013 and again in late 2014, but
then appeared in abundance starting in mid-2016, laid egg strings in October 2016 and April, Octo-
ber and November 2017 (JG, personal observations), and has persisted through 2017 (Figure 4).
Berthellina ilisima (Ev. Marcus and Er. Marcus, 1967). Ellwood Mesa Reef, 1 specimen,
13 m depth, 2 November 2016; 3 specimens, 13 m depth, 11 January 2017 (C. Pierre, personal
communication to JG, 6 October 2016). Living specimens were held at the Marine Science Insti-
tute, UCSB, and observed by JG, 6 October 2017. Anacapa Is, 1 specimen, intertidal, 22 May 2018
(Taylor 2018).
GODDARD ET AL.: EL NIÑO IMPACT ON HETEROBRANCH SEA SLUG RANGES 121
FIGURE 4. Abundance of the Bulla gouldiana and Aplysia vaccaria in the low rocky intertidal at Naples, Santa
Barbara, California 2006–2017.
Remarks: Berthellina ilisima was reported from Naples Reef by Behrens (1991 [as B. engeli]),
where it was found again by Shane Anderson of UCSB in October 1999, collected, and its devel-
opment to hatching documented by Goddard and Hermosillo (2008).
Polycera alabe Collier and Farmer, 1964. Anacapa Island, California, 1 specimen, 23 m depth,
north side of West Is., 18 December 2015 (D. Klug, personal communication to JG, 24 January
2016; for image see Klug 2015).
Remarks: The specimen observed by Klug (2015) matches variation A pictured by Behrens
and Hermosillo (2005) and Hermosillo et al. (2006) and considered to be P. alabe by Pola et al.
(2014). It was found 4.5 km west of Cathedral Cove, on the north side of East Anacapa Island,
where one specimen of P. alabe was found during the 1997-98 El Niño (Engle and Richards 2001).
Atagema alba (O’Donoghue, 1927). Monterey Breakwater, Monterey, California, 1 specimen,
6 m depth, 20 August 2016 (P. Webster, personal communication to JG, with image, 23 August
2016). Carmel Point, Carmel, California, 1 specimen, 45 mm long, low rocky intertidal, 27 June
2017 (observed by JG; for image see <https://www.inaturalist.org/observations/6834885>).
Remarks: MacFarland (1966) reported the collection of 4 specimens of this species (as
Petelodoris spongicola MacFarland, new species) from the Monterey Peninsula in 1908.
Aldisa sanguinea (Cooper, 1863), Otter Crest, Oregon, 2 specimens, under low rocky inter-
tidal ledges, 3 June 2016 (observed by JG).
Remarks: Each of the above specimens were red and had two spots on the middle of the dor-
sum. Goddard (1997) reported finding 3 specimens of A. sanguinea at Otter Crest, which was the
northernmost locality for the species until specimens were reported from Campbell River, on the
east coast of Vancouver Island and Scott’s Bay, Barkley Sound, on the west coast of Vancouver
Island, British Columbia by Wakeling (2005) and Penney (2005), respectively.
Baptodoris mimetica Gosliner, 1991. Carmel Point, California, 1 specimen, low rocky inter-
tidal 27 June 2017 (observed by JG; for image see <https://www.inaturalist.org/
observations/6834892>).
Remarks: The published northern limit for this species is Santa Cruz, California (Gosliner
1991). However JG found one specimen in the low rocky intertidal at Salt Point, Sonoma Co.,
California in July 2010; for image see <https://www.inaturalist.org/observations/2941658>.
Jorunna pardus Behrens and Henderson, 1981. Anacapa Island, California, 1 specimen, sub-
tidal, off the west end of the West Anacapa, 7 October 2016 (Klug 2016b), and 1 specimen, sub-
tidal, off the north side of Middle Anacapa, 29 December 2016 (Klug 2016c).
Remarks: Behrens and Henderson (1981) noted 7 specimens from Anacapa Island, which has
remained the northernmost known locality for this species.
Taringa aivica Ev. Marcus and Er. Marcus, 1967. La Jolla Shores, California, 1 specimen
found by John Huber at an unspecified depth, 8 August 2016 (Doyle 2016). Mission Bay, San
Diego, California, 1 specimen, 2 m depth, 14 June 2018 (Fig. 3C) (observed by CH).
Remarks: These are the first documented sightings of this Panamic species in the Southern
California Bight since Behrens and Henderson (1982) reported finding a single specimen at 10 m
depth in Paradise Cove, Malibu in April 1979. Paradise Cove remains the northernmost known
locality for T. aivica.
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Felimare porterae (Cockerell, 1901). Pacific Grove, Monterey Co., California, 1 specimen,
subtidal, 27 June 2017 (Gerakin 2017). Carmel Pinnacles, Monterey Co., California, 2 specimens,
46 m depth, 24 September 2016 (C. Bauder, personal communication to JG 29 September 2016;
for image see <http://www.baue.org/images/galleries/v/local/Lunaticos_9-24-16/>). Point Sierra
Nevada, San Luis Obispo Co., California, 1 specimen, 29 January 2018 (observed by JG; see
<https://www.inaturalist.org/observations/9698537>). Near Point Buchon, San Luis Obispo Co.,
California, 1 specimen [as Mexichromis porterae], subtidal, 29 July 2016 (Harmer 2016). Cave
Landing, San Luis Obispo Co., California, 1 specimen, 17 mm long crawling, 4 December 2017
(observed by JG; for image see <https://www.inaturalist.org/observations/9057952>).
Remarks: Felimare porterae was found on the Monterey Peninsula for the first time in 1894
(MacFarland 1905 [as Chromodoris porterae]). It has been found only a few times in that area
since (MacFarland 1966; GM, personal observations; for image see <https://www.inaturalist.org/
observations/845636>), and has not been reported from farther north. Additionally, Harmer’s
(2016) image represents only the second time F. porterae has been found in San Luis Obispo Co.,
the first was during subtidal monitoring conducted from 1976 to 2001 as part of studies on the
effects of the thermal discharge by the nuclear power plant at Diablo Canyon, (D. Behrens, per-
sonal communication, with unpublished manuscript, to JG, 29 January 2006; also see Steinbeck et
al. 2005). Felimare porterae is a Californian species usually found south of the Palos Verdes penin-
sula.
Diaphoreolis lagunae (O’Donoghue, 1926). Whiskey Creek, Curry Co., Oregon, low rocky
intertidal, 2 specimens, 16 June 2015 (observed by JG et al.), and 1 specimen (Fig. 3D), 29 May
2017 (observed by NT).
Remarks: Diaphoreolis lagunae has been recorded previously in Oregon only three times,
twice (July 1987 and June 1995) from Whiskey Creek (Goddard 1990, 1991 [as Cuthona lagunae],
personal observations) during strong and moderate El Niño events, respectively, and once (June
1996) from 48 km north in the low rocky intertidal on the south side of Humbug Mountain (God-
dard 1997, CASIZ 107440) during a weak La Niña following a moderate El Niño. Goddard (1991,
p. 152) also recorded one specimen from the low rocky intertidal near Crescent City, California in
July 1998, during the strong 1997-98 El Niño.
Flabellina cooperi (Cockerell, 1901). Fitzgerald Marine Reserve, San Mateo Co., California,
low rocky intertidal, 1 specimen, 20 June 2016 (observed by RA; for image see <https://www.
inaturalist.org/observations/3492678>).
Remarks: Flabellina cooperi is known as far north as Coleman Beach, Sonoma Co., Califor-
nia (Goddard et al. 2016)
Flabellinopsis iodinea (Cooper, 1863). Cape Flattery, Washington, subtidal, At least 10 spec-
imens observed and photographed by Karin Fletcher and Doug Miller on 6 dates, August 2015
(Pacific Northwest Shell Club 2016 [as Flabellina iodinea]).
Remarks: Flabellinopsis iodinea has been found north to Vancouver Island, British Columbia
(Bernard 1970; and see Goddard et al. 2016)
DISCUSSION
During and in the two years following the 2015–16 El Niño 37 species of heterobranch sea
slugs were recorded north of their usual ranges, a total similar to the 30 total listed by Goddard et
al. (2016) for the 2014-15 warm anomaly in the Northeast Pacific Ocean. However, the 23 species
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found at new northernmost localities in the current study and Merlo et al. (2018) is more than dou-
ble the number reported by Goddard et al. (2016), and their mean range extension was 270 km, or
79% longer. While taxonomic splits since 2016 (Lindsay and Valdés 2016; Uribe et al 2017)
account for the addition of two species (Limacia mcdonaldi and Hermissenda opalescens) to the
recent total, the 2015-16 El Niño clearly had a significant effect on heterobranch distributions in
the region.
Of the 37 species treated herein, 22 were not among the species covered by Goddard et al.
(2016). The combined 2014–17 marine heat wave in the Northeast Pacific Ocean therefore drove
range shifts in at least 52 species of benthic heterobranchs, approximately one quarter of the
species known from the Californian and Oregonian biogeographic provinces (Behrens and Her-
mosillo 2005). Thirty of the 52 were found farther north than ever observed before. Although clear-
ly significant and likely unprecedented, it is difficult to directly compare these numbers to those
observed during warm-water events of the last half century, owing to (1) historical gaps in sam-
pling coverage, (2) lack of dates for some of the earlier records, (3) recent taxonomic revisions, and
(4) increased numbers of observers, especially citizen scientists, combined with increased oppor-
tunities for posting online geo-referenced observations accompanied by images. As evidenced by
the number of known northern range limits that were not surpassed by species we found in our
studies, many have been advected as larvae and settled as far north before, especially during strong
El Niño events. These include, for example, Bulla gouldiana, Aplysia californica, Berthellina ilisi-
ma, Polycera alabe, Dirona picta, the chromodorids Felimare porterae and Felimida macfarlandi,
and Flabellinopsis iodinea (Goddard et al. 2016; present study and references therein). However,
the range shifts since late 2013 by species like Okenia rosacea, Carminodoris bramale, Doriopsil-
la fulva, Anteaeolidiella oliviae, Noumeaella rubrofasciata, and Phidiana hiltoni are unprecedent-
ed, either in geographic extent or population density, with their prior absence from new northern
ranges backed by historical records.
The sheer number of heterobranch range shifts associated with the 2014–17 marine heat wave,
especially those to new northernmost localities, begs questions about the possible role of global
warming, beyond simple temperature increases in the California Current System and Northeast
Pacific, which so far have been less than in other ocean regions (Cheng et al. 2017). Dispropor-
tionate Arctic warming, or “Arctic amplification,” has been implicated in slowing the Northern
Hemisphere polar jet stream, making it wavier, with more persistent high pressure ridges and low
pressure troughs (Francis and Vavrus 2015; Francis et al. 2017). This increased amplitude and per-
sistence is reflected in the North Pacific Oscillation (NPO), a leading pattern of atmospheric vari-
ability. A persistent atmospheric ridge was observed over the Northeast Pacific during winter 2013-
2014, which by altering wind stress and reducing the depth of the mixed layer generated the 2014
warm anomaly in sea-surface temperatures (Bond et al. 2015). Atmospheric teleconnections
between the North Pacific and tropical Pacific and back again are then thought to have effectively
forced phase changes in the Northeast Pacific reflected first in the North Pacific Gyre Oscillation
(NPGO), then the Pacific Decadal Oscillation (PDO), and ultimately the El Niño Southern Oscil-
lation (ENSO) (Di Lorenzo and Mantua 2016; and see Levine and McPhaden 2016). The direction
of the observed phase changes are known to be associated with, among other effects, reduced
coastal upwelling and increased poleward and onshore transport of coastal waters in the NE Pacif-
ic, which can advect planktonic propagules and pelagic organisms poleward, well beyond their
usual ranges (e.g., Lluch-Belda et al. 2005; Ohman et al. 2017). Global warming, by increasing the
amplitude and persistence of the NPO, therefore appears to be important in driving increased pole-
ward range shifts. The unprecedented magnitude and duration of the 2014–17 marine heat wave
likely also contributed to the continued presence at outer coast sites of recently arrived southern
heterobranchs such as Okenia rosacea, Doriopsilla fulva, and Hermissenda opalescens in Oregon
and Phidiana hiltoni in northern California by keeping open thermal windows conducive to
growth, reproduction and development.
At Naples, an outer coast site in the northern part of the Southern California Bight, Bulla goul-
diana was present for about one year after first appearing (Figure 4), while to the north at Morro
Bay, B. gouldiana continues to be present after at least two years. Southern species may persist
longer in embayments compared to nearby outer coast sites, owing to elevated summer tempera-
tures on the one hand, and increased potential for larval retention and local recruitment on the
other, thus allowing for reproduction and completion of life cycles in the bays. With the return to
ENSO-neutral conditions and more normal sea-surface temperatures in the NE Pacific Ocean, it
will be interesting to see how long southern species like Bulla gouldiana, Aplysia californica,
A. vaccaria, and Doriopsilla fulva persist in northern embayments.
Site-specific topography aside, with global ocean temperatures steadily increasing in the back-
ground, recently settled southern species are likely to persist longer in their recently expanded
northern ranges, especially compared to historically more ephemeral ENSO-driven range shifts
(reviewed by Lluch-Belda et al. 2005). So far this appears to be the case for Okenia rosacea,
Doriopsilla fulva, D. gemela, Felimida macfarlandi, Doto form A, Janolus anulatus, and
Fla-bellina cooperi, all of which were found in 2017 at or near range limits reached a year or two
earlier (Goddard et al. 2016; present study). However, other range shifts documented by Goddard
et al. (2016) appear to have been short-lived, with no northern sightings since 2015 of Placida
brookae McCarthy, Krug and Valdés 2017 (formerly P. cremoniana), Trapania velox, Hancockia
californica MacFarland, 1923, Anteaeolidiella chromosoma (Cockerell and Eliot, 1905), and
Emarcusia morroensis Roller, 1972. Phidiana hiltoni, which has been taking smaller geographic
steps with its lecithotrophic larvae, has yet to retreat from any new range acquired since 1977 and
remains the best documented example of a permanent northern range shift among Northeast Pacif-
ic heterobranchs (Goddard et al. 2011; present study; King et al. in prep).
In central California southward range shifts by nudibranchs with more northern distributions
were last observed during the strong La Niña events of 2007–08 and 2010–11 (e.g., Aldisa albo-
marginata Millen in Millen and Gosliner, 1985, Aldisa cooperi, Robilliard and Baba, 1972, Diaul-
ula lentiginosa (Millen, 1982), and Doris odhneri (MacFarland, 1966) subtidally off the Monterey
Peninsula [see records at <http://www.baue.org/images/galleries/v/FieldGuide/Opistho
branchs/>], and Janolus fuscus (O’Donoghue, 1924) intertidally in San Luis Obispo Co. [JG
personal observations, CASIZ 186479]). We did not observe any southern range shifts during the
2014–17 marine heat wave, and the only record of a more northerly species penetrating central
California we are aware of during this period is of Dirona albolineata MacFarland in Cockerell and
Eliot, 1905 at Pillar Point (<https://www.inaturalist.org/observations/1727582>). The last time
D. albolineata was recorded farther south was during the 2009–10 La Niña, by GM at Carmel
Point, on the Monterey Peninsula (for image see <https://www.inaturalist.org/observations/
834800>).
As the oceans continue to warm we expect more poleward range shifts by heterobranchs to
become permanent, and likely lead to complex and unexpected changes in shallow-water benthic
encrusting and fouling communities.
ACKNOWLEDGMENTS
For assistance in the field we thank Will and Ziggy Goddard, Katy Kennedy, Sawyer Reid,
Zach Taylor, Kara Termulo, Spencer Dybdahl-Riffle, Hans Bertsch, and Josh Hallas. JG thanks
GODDARD ET AL.: EL NIÑO IMPACT ON HETEROBRANCH SEA SLUG RANGES 125
126 PROCEEDINGS OF THE CALIFORNIA ACADEMY OF SCIENCES
Series 4, Volume 65, 28 Sept. 2018, No. 3
Constance Goddard and Jerry and Lynn Rudy for their hospitality on the northern California coast.
We are grateful to Clinton Bauder, Kenan Chan, Todd Cliff, Colby Davidson, Brandon Exner,
Karin Fletcher and Doug Miller, Phil Garner and Merry Passage, Andrew Harmer, Jackie Hilder-
ing, Douglas Klug, David Kushner, Lillian Mayer, Peter Mieras, Andy Murray, Phil Nosler, Joshua
Sprague, Chad Tamis, and Patrick Webster for sharing data and images of their nudibranch finds,
and Liz Kools for her ongoing assistance at the California Academy of Sciences. We especially
thank Karin Fletcher and Andy Lamb for forwarding reports of unusual occurrence from the Pacif-
ic Northwest which we otherwise likely would have missed. Finally, we thank Hans Bertsch and
Ángel Valdés for reviewing and improving the manuscript.
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