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NAUTILUS

Volume 134, Number 2

August 4, 2020

ISSN 0028-1344

JUN 0 8 2022

CONTENTS LIBRARIES =

Rese

Cynthia M. Asorey Architectonica karsteni Rutsch, 1934 (Gastropoda: Architectonicidae) in

Javier Sellanes seamounts of the Nazca-Desventuradas Marine Park: First record in

Erin E. Easton Ciena Avalers SING ene EN MOO Tie so 8 ios aes se lige Brees ode Shed sat emcee a ee 61

Ridiger Bieler

Ariadna Mecho

Hans Bertsch A history of eastern Pacific marine heterobranch: researclaw.e ices ve |

RESEARCH NOTES

Gabriel A. Delgado First ex-situ observation of Vasula deltoidea (Lamarck, 1822) (Gastropoda:

Einat Sandbank Muricidae) mating and egg-laying with emphasis on the potential for

William C. Sharp hatchery-reared individuals to aid coral reef restoration... 89

Michael Middlebrooks Range and dietary expansion of the nudibranch Felimare ruthae

Daniela Gutierrez-Andrade (Ev. Marcus and Hughes, 1972) (Gastropoda: Chromodorididae) ................++ 92,

Sarah E. Cuccinello

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THE NAUTILUS 134(2):61—70, 2020

Page 61

Architectonica karsteni Rutsch, 1934 (Gastropoda:

Architectonicidae) in seamounts of the Nazca-Desventuradas

Marine Park: First record in Chilean waters since the Miocene

Cynthia M. Asorey

Departamento de

Biologia Marina

Facultad de

Ciencias del Mar

Universidad Catoélica

Departamento de Biologia

Marina, Facultad de

Ciencias del Mar

Universidad Catoélica del

Norte, Coquimbo

del Norte CHILE

Coquimbo, CHILE and

and Sala de Colecciones

Sala de Colecciones Biol6gicas

Bioldgicas Universidad Cato6lica

Universidad del Norte

Catélica del Norte

Coquimbo, CHILE

Javier Sellanes' Erin E. Easton”

Millennium Nucleus

Ecology and

Sustainable

Management of

Oceanic Island

Universidad

Catolica del Norte

Coquimbo, CHILE

Ariadna Mecho

Millennium Nucleus

Ecology and

Sustainable

Management of

Oceanic Island

Universidad

Catoélica del Norte

Coquimbo, CHILE

Riidiger Bieler

Negaunee Integrative

Research Center

Field Museum of

Natural History

Chicago, USA

ABSTRACT

Eight species of Architectonicidae have been reported for

lower Miocene deposits in continental Chile. One of these

species is Architectonica karsteni, which had an inferred

geographic range, for this epoch, extending from Costa Rica to

central Chile (~8° N to 34° S), and even in the Caribbean.

There is no evidence of the current presence of the family

immediately off the coast of Chile. We report the discovery

of living specimens and shells of A. karsteni at four seamounts

at ~200 m water depth in the recently created Nazca—

Desventuradas Marine Park, located ~900 km west of Chile.

Morphological identification was based on protoconch diam-

eter, coloration patterns, and teleoconch sculpture. We also

provide sequence data for portions of the mitochondrial

COI and 16S rRNA genes as a contribution toward future

population-level and phylogenetic analyses of this poorly

known group. Insight on the habitat of the species based on

underwater imagery is also provided. This new record extends

the geographic distribution of A. karsteni ~20° southward from

its current recorded range (i.e., Baja California to Peru). The

finding of this species contributes to the knowledge of the

fauna of these seamounts, and ultimately informs and boosts

conservation efforts of these relatively pristine habitats.

Additional Keywords: Benthos, mesophotic zone, biogeography,

Southeast Pacific Ocean, sundial shell, COI, 16S rRNA

! Author for Correspondence: [email protected]

2 Present address: School of Earth, Environmental and Marine

Sciences, University of Texas Rio Grande Valley, Brownsville,

TX, USA

INTRODUCTION

Architectonicidae (commonly called “sundials”) are a

family of subtropical to tropical marine gastropods (Bieler,

1984). Their shell shape typically ranges from trochoidal

to discoidal with a basal-centered umbilicus, but it may on

occasion be planispiral with disjunct whorls. They are

characterized by a hyperstrophic protoconch with the

apex projected into the teleoconch umbilicus (Bieler,

1993). Architectonicids have planktotrophic larvae with

larval durations that range from several weeks to several

months (Robertson, 1967). Long duration of larval life

allows the larvae to be displaced by currents over large

distances (sometimes 1000s of km), therefore enabling

them to maintain the wide geographical distributions

reported for some species of this family (Bieler and Petit,

2005). For instance, several species, such as Archi-

tectonica perspectiva (Linnaeus, 1758) and Heliacus

variegatus (Gmelin, 1791), have extremely wide geo-

graphic ranges, extending from the east coast of Africa

(Indian Ocean) to the islands of the Central Pacific

(Bieler, 1993). A few of them, including Heliacus tro-

choides (Gmelin, 1791) and Psilaxis radiatus (Roding,

1798), are known to extend to the eastern Pacific coast

from the Indo-West and Central Pacific (Robertson, 1976,

1979). The distribution of architectonicid species may be

limited by the temperature requirements of their cni-

darian prey more than by their own tolerance (Bieler,

1993), since architectonicid larvae have been collected at

water temperatures as low as 13.5 °C (Scheltema, 1971),

and adults collected alive in deep waters at temperatures

as low as 2.4 °C (Bieler, 1993). Changes in oceanographic

Page 62

conditions, current patterns, and/or availability of prey

may therefore have caused many species to have suffered

reductions in their range of geographical distribution and

to become extinct at high latitudes during the Miocene

(Frassinetti and Covacevich, 1981; Nielsen and Frassinetti,

2007). For example, Pseudotorinia obtusa (Bronn, 1831) is

known as a Neogene fossil from the North Sea (Janse and

Janssen, 1983), has no extant representatives in that ocean

(Melone and Taviani, 1984).

Such extinctions and contractions in geographic ranges

have resulted in only two extant species of Architectonicidae

having a known range that extends into Chilean waters.

However, these species, Heliacus implexus (Mighels, 1845)

and Spirolaxis cornuarietis (Bieler, 1993), are only known

from Rapa Nui (Easter Island), which is ~3700 km west of

continental Chile (Rehder, 1980; Bieler, 1993; Osorio,

2018). Nevertheless, samples collected from the Navidad

Formation (~34° S, Figure 1), Ranquil Formation (~36.6°

S) and Lemo Island (~44.64° S) reveal that at least eight

species of the family were present in Chile during the lower

Miocene (Frassinetti and Covacevich, 1981; Nielsen and

Frassinetti, 2007). These species include: Architectonica

karsteni, Intitectonica inti Frassinetti and Covacevich, 1982,

Discotectonica navidensis Frassinetti and Covacevich, 1982,

Heliacus (Torinista) taverai Frassinetti and Covacevich,

1981, Heliacus (Torinista) bahamondei Frassinetti and

Covacevich, 1981, Heliacus (Torinista) chonos Nielsen

and Frassinetti, 2007, and Solatisonax bieleri Nielsen and

Frassinetti, 2007.

Architectonica karsteni was described by Rutsch (1934)

from the Miocene Cantaure Fomation of northern

Venezuela as a subspecies of Architectonica nobilis

| | Miocene records

|| Previously known distribution

Wx New records

Pacific Ocean

SF9 Ses +s. lc wl a

Desventuradas is.

Lt iv

-160 -140

-120

THE NAUTILUS, Vol. 134, No. 2

Roding, 1798. It was first reported for Chile as part of the

fossil record of the Miocene by Frassinetti and Covacevich

(1981). Additional records revealed that A. karsteni was

consistently present in the lower Miocene fossil record in

Central Chile and fossil records from the Miocene and

Miocene-Pliocene boundary in Mexico (~16° N) ( Bése,

1906), Venezuela and Grenadine Islands (DeVries, 1985;

Nielsen and Frassinetti, 2007) (Figure 1). These records

suggest that the geographic range of A. karsteni during the

Miocene spanned the east Pacific and even the Caribbean

Sea coasts, a wider longitudinal distribution relative to its

current distribution. The present range of the species

extends from Baja California (~32° N) to Pert (~5° S)

(Figure 1) at 50 to 190 m depth on a variety of substrata

(e.g., mud, fine sand, shells, gravel) (DeVries, 1985;

Bieler, 1993). No records of living A. karsteni have been

reported so far for the Pacific Ocean south of 5°S, the

Caribbean Sea or the Atlantic (Bieler, 1993).

In this paper, we report the presence of A. karsteni at

four seamounts near the junction of the Salas y Gomez

and Nazca Ridges (Figure 1) (~25° S, 82° W) within

the newly created Nazca-Desventuradas Marine Park

(NDMP), Chile. In addition, we provide sequence data

for the barcode regions of the mitochondrial (mt) 16S

ribosomal RNA (rrnaL) and cytochrome oxidase I (COI)

genes of A. karsteni and present them in a phylogenetic

context with the only four Architectonicidae species

with COI or 16S barcode data: Architectonica per-

spectiva (COI, 16S), A. maxima (16S), Philippia lutea

(COI), and Psilaxis radiatus (16S). A description of the

habitat of the species based on underwater imagery is

also provided.

South :

America

mf 0 2000 Km _ | -40

sR | i

400 80 ‘among.

Figure 1. Modern and Miocene geographic distribution of Architectonica karsteni and locations of the new records reported here.

Live specimens were only collected from seamount SF.5.

C.M. Asorey et al., 2020

MATERIALS AND METHODS

Study Area: From October to November 2016, a mul-

tidisciplinary oceanographic cruise (CIMAR 22 “Oceanic

Islands”) was carried out onboard the research vessel

AGS61 CABO DE HORNOS. The aim of the cruise was to

study the benthic habitats and fauna of unexplored sea-

mounts of the Juan Fernandez and Desventuradas

Ecoregion (Spalding et al., 2007). The northern extent of

this ecoregion falls within the lower Miocene latitudinal

range of Architectonica karsteni and includes the islands

of the Desventuradas and the surrounding seamounts,

which are part of the 144 seamounts of the Nazca and

Salas y Gémez Ridges. The Salas y Gomez Ridge is a long

and narrow seamount chain stretching from the East

Pacific Rise (west of Easter Island in the Easter Island

Ecoregion) at ~27°01° S, 111°00° W to just west of the

Desventuradas Islands at ~25° 27 “S, 81°43’ W, where it

merges with the Nazca Ridge. This latter stretches in a

northeastern direction to ~17°43’ S, 78°07’ W (Parin

et al., 1997: Galvez Larach, 2009). Of these seamounts, 21

are in the Chilean exclusive economic zone (FEZ) around

the Desventuradas (Yafiez et al., 2009). Prior to this study,

benthic habitats of the seamounts within the EEZ sur-

rounding the Desventuradas had not been explored.

Some of the adjacent seamounts at the junction of these

two ridges were surveyed in the 1970s and 1980s (Parin

et al., 1997; Mironov et al., 2006). Such surveys revealed

that these seamounts are characterized by a highly en-

demic fauna with well-expressed Indo-West Pacific af-

finities, with only the easternmost seamounts having some

species with affinities to the fauna of the adjacent con-

tinental coast of South America (Parin, 1991).

Samples Collection: Within the NDMP, the slopes of

San Ambrosio and San Felix islands (i.e., Desventuradas

Islands) and summits of six seamounts were surveyed

using a remotely operated vehicle (ROV) and a modified

Agassiz trawl. Unless weather or sea conditions precluded

the use of one of the survey methods, the protocol for

the benthic survey consisted of a visual survey of the

study site using an ROV (Commander MK2; Mariscope

Meerestechnik, Kiel, Germany) equipped with a HD

Camcorder (Panasonic SD 909) and laser pointers (10 cm

Page 63

apart) followed by sampling with the Agassiz trawl. The

latter consisted of a metal frame with an opening of

1.5m X 0.5 m (width X height) fitted with a net of 12 mm

mesh at the cod end, operated in 10 min hauls (bottom

contact) at ~2 knots. Collected specimens were preserved

in 100% ethanol and voucher specimens deposited in the

biological collections of the Universidad Catélica del Norte

(SCBUCN). Sample collection was performed under

permission Res. Ext N°41/2016 from SERNAPESCA

(Chile) to Universidad Catélica del Norte. This resolution

authorizes us to collect species throughout the NDMP area

until October 2020.

Taxonomic Identification: Identification of the seven

empty shells and three living specimens of architectoni-

cids (Table 1) was made according to Bieler (1993). The

teleoconch sculpture and protoconch diameter of one

living specimen (ID number SCBUCN 6928a) was ex-

amined with a Hitachi SU3500 scanning electron mi-

croscope (SEM) at the Microscopy Laboratory of the

Facultad de Ciencias del Mar, Universidad Catoélica del

Norte, Coquimbo, Chile. The shell was dried in a labo-

ratory drying oven at 65°C for 24 h and mounted on

bronze stubs without metal coating.

Molecular Data: Whole genomic DNA was isolated

from the muscle tissue of the foot of a specimen (ID

number SCBUCN 6950) with the GeneJET Genomic

DNA Purification Kit (ThermoFisher Scientific Waltham,

MA) per manufacture’s protocol and submitted to Bio-

polymers Facility at Harvard Medical School for library

preparation and next-generation sequencing (NextSeq

500). Trimmed reads (Trimmomatic-0.32, Bolger et al.,

2014) were assembled de novo with SPAdes (Bankevich

et al., 2012) on the University of New Hampshire Bio-

informatics Core facility RON server. The resulting

SPAdes contig consensus sequences were blasted (Blastn)

against the reference mitochondrial genomes in GenBank

to identify which of the contigs corresponded to the

mitochondrial genome of A. karsteni. After circularizing

and editing overlapping ends of the identified SPAdes

contig in Geneious R11.1.5 (Kearse et al., 2012), trimmed

reads (BBDuk v. 37.25) were mapped to this reference

sequence in Geneious and reviewed manually for quality

Table 1. Locations and depth of the seamounts sampled; and identification and measurements (diameter and height) of the

Architectonica karsteni shells.

Station Latitude Longitude Depth (m) ID number SCBUCN Diameter (mm) Height (mm) Sample alive

SF.5 LWA —81.8806° 180 6928a 28.4 1 Yes

6950 Lie) ti 2 No

6926 a 10.2 No

SF.5.029* 26.8 TAT No

SF .5,027* 28.4 14.0 Yes

6928b Bis 15.3 Yes

6921 24.9 It No

SF.6 ewe ele —§2.3963° Lo 7066 31.4 Lye No

SF.9 = at Lie 83 Oa” 200 6913 14.3 6.4 No

$21 ca a) —79.8893° 150 vig ere 31.9 18.0 No

* Samples that do not have SCBUCN numbers, only field-assigned IDs

Page 64

control (e.g., to confirm read coverage was sufficient,

=10). The resulting consensus sequence was used to

annotate the mitochondrial genome based on annota-

tions identified by MITOS (Bernt et al., 2013) with gene

boundaries manually adjusted based on alignment of in-

dividual genes with the gastropod Siphonaria gigas ref-

erence mitochondrial genome (NC_016188).

The complete COI and 16S rRNA sequences were

uploaded to GenBank (MN270389 and MN270388, re-

spectively) and aligned separately with default MUSCLE

(Edgar, 2004) parameters to all Architectonicidae sequences

available in GenBank. Because only two Architectonicidae

species, Architectonica perspectiva (FJ917269) and Philippia

lutea (AY29684:3), had COI sequences available in GenBank,

we also included four species belonging to two supertamilies

assumed closest to Architectonicoidea (Dinapoli and

Klussmann-Kolb, 2010): Omalogyroidea (Omalogyra fusca -

FJ917272, Omalogyra sp. - FJ917273) and Valvatoidea

(Valvata piscinalis - F]917267, Cornirostra pellucida -

FJ917282). For the alignment of 165 rRNA sequences, 50

haplotypes of Architectonicidae sp. (MH557974 to

MH558023) were available in addition to one sequence

each from A. perspectiva (FJ917251), A. maxima (KP252986)

and Psilaxis radiatus (AY081999). Prior to reconstruction of

the phylogeny, alignments were trimmed to the shortest

region with sequence data for all individuals. Because the

available COI sequence for P. lutea (623 bp) is from a dif-

ferent section of the gene than A. perspectiva (577 bp) and the

four other species used to construct the phylogeny, there was

only 322 bp of overlap for all sequences. Therefore, P. lutea

was included in alignments to determine pairwise divergences

compared with A. karsteni, but it was removed from the

phylogenetic tree construction. The resulting alignments

were used to construct the respective phylogenetic trees

with PhyML 3.0 (Guindon et al., 2010) Geneious plugin,

with the following settings: bootstrap replicates = 1000,

optimize = Topology/length/rates, Topology search = NNI,

nucleotide model substitution = GTR. Significant boot-

strap values (=90) are reported at the nodes.

RESULTS

Samples and Habitat Description: A total of seven

empty shells and three living Architectonica karsteni

specimens were collected at four stations within the

NDMP (Table 1); however, live specimens were only

collected from seamount SF.5 (Figure 1). The smallest

shell measured 14.3 mm in diameter and the two largest

measured 28.4 mm in diameter. Although 4 to 15 other

mollusk species were found at each of the four collection

sites, species that co-occurred with A. karsteni at three or

more sites were Atrimitra isolata (Sellanes and Salisbury,

2019) (Mitridae) and Chryseofusus kazdailisi (Fraussen

and Hadorn, 2000) (Fasciolariidae), which were collected

at SF.5, SF.6, and SF.9 seamounts; as well as empty

shells of the bivalve Tucetona kauaia (Dall, Bartsch, and

Rehder, 1938) (Glycymerididae), which were collected at

SF.5, SF.9 and S21 seamounts. Of the four seamounts in

THE NAUTILUS, Vol. 134, No. 2

which A. karsteni was collected, three (SF.6, SF.9 and

S21) were also studied via ROV surveys. Benthic habitats

at SF.6 and SF.9 were dominated by coarse sand and the

presence of maérl-rhodoliths, and scattered rocky outcrops

were also spotted at these sites (Figures 2-5). The bottom

at S21 was dominated by finer sand (Figures 6—7). Wind

and current conditions prevented the deployment of the

ROV at SF.5, where the live specimens were collected.

Shell Morphology: Shells of live collected specimens

have the characteristic yellowish-red marbled color pat-

tern of the species (Figures 8-9) (Bieler, 1993). Sub-

sutural and peripheral ribs are whitish with more or less

irregular brown blotches (about 10-16 on 4th whorl of

upper peripheral rib, each 1-2 nodules wide); mid ribs are

light-brown or bluish-grey, weakly mottled with brown;

the basal field is light-brown or bluish-grey with 5-6

dotted or relatively solid spiral lines (marking the reduced

spiral ribs of the basal field), wider towards the umbilicus.

The umbilical carinae are whitish with a light- to dark-

brown marbled pattern. In contrast, most of the empty

shells showed a uniform greenish yellow color due to loss

of color and different degrees of erosion, although all of

them were distinguishable as A. karsteni because the

distinctive architecture of the shell was sufficiently con-

served for species assignment.

Shell morphology of all samples were consistent with

the description published by Bieler (1993). Only one

specimen had its protoconch measured, because the

protoconch of most of the other specimens showed a high

degree of erosion, precluding accurate measurements.

Even in the photographed specimen, it was difficult to

distinguish the boundary between the end of the proto-

conch, the “stage of arrested growth” and the beginning of

the teleoconch (Figure 11). The protoconch of specimen

SCBUCN 6928a measures 943 wm (Figure 11) and is

whitish to light-brown in color.

COI and 16S rRNA Data: The only sequence data

available in GenBank for Architectonicidae species are

COI, 16S, and nuclear 18S and 28S rRNA genes for

Architectonica perspectiva: 16S for A. maxima; COI, 28S,

and nuclear Histone 3 (H3), U2 and small nuclear RNA

for Philippia lutea, 16S for Psilaxis radiatus and H3 for

Heliacus variegatus: At the level of uncorrected nucleo-

tide substitutions, A. karsteni was 18.6% divergent from

both A. perspectiva and P. lutea. However, the amino acid

sequence of A. karsteni was identical to that of A. per-

spectiva, whereas these species differed from P. lutea by 3

amino acids (2.80%). The percentage divergence based on

nucleotide substitutions was 17.63% across the complete

573 bp alignment of A. perspectiva and A. karsteni and the

translated amino acid sequence differed by one (0.52%)

change of Val to Ile. Divergence based on nucleotide

substitutions was 17.98% across the 623 bp alignment of

P. lutea and A. karsteni and the amino acid sequences

differed by six positions (2.90%). The phylogenetic tree

reconstructed based on the 580 bp COI alignment shows

A. karsteni sister to A. perspectiva and Architectonicoidea

sister to Omalogyroidea, which together are sister to

Valvatoidea with a strong (>98) bootstrap support

C.M. Asorey et al., 2020

Page 65

Figures 2-7. Panoramic and zoomed-in images taken with an ROV at the summit seamounts where Architectonica karsteni was found. 2.

Panoramic view of SF.6, illustrating the continuous homogeneous bottom of coarse sand with little relief and dominated by sea urchins

(Scrippsechinus fisheri) and sea anemones (Cerianthidae). 3. Zoomed in view of sea anemones (Hormathia sp. and Cerianthidae) and

polychaete tubes (Eunice sp.) on SF.6. 4. Panoramic view of SF.9, illustrating the continuous homogeneous bottom of coarse sand with little

relief and clusters of maérl-rhodoliths, dominated by sea anemones (Cerianthidae). 5. Zoomed-in view of sea anemones (Cerianthidae),

polychaete tubes (Eunice sp.) and sponges on SF.9. 6. Panoramic view of S21, illustrating the presence of sea anemones (Hormathia sp.), sea

pens (Protoptilum sp.), sand dollars (Clypeaster isolatus) and sea urchins (Scrippsechinus fisheri) on the continuous homogenous sandy

bottom. 7. Zoomed-in view of sea anemones (Hormathia sp.) on $21. Scale bars = 10 cm. Photo credits: Mathias Gorny /Jan M. Tapia.

(Figure 12). The 415 bp alignment and phylogenetic tree

based on 16S rRNA sequence data revealed that none of

the other Architectonicidae spp. had the same haplotype

as A. karsteni, which differed by at least 17.28% from the

most similar haplotype (Architectonicidae sp. - MH557975);

A. karsteni was 19.53% divergent from Psilaxis radiatus, the

most similar haplotype belonging to a specimen assigned

to species level. Because most of the GenBank sequences

belong to indeterminate species of Architectonicidae, little

additional information can be extracted from the resulting

phylogenetic tree (Figure 13).

DISCUSSION

Information about the invertebrate benthic fauna

inhabiting seamounts of the Salas y Gémez and Nazca

Ridges is scarce, and most of it is associated with studies

carried out between 1973 and 1987 (Mironov and

Detinova, 1990; Parin et al., 1997). Parin et al. (1997)

reviewed the fauna for 22 seamounts, from which they

reported one species of Polyplacophora, 27 species of

Gastropoda (most of them of the superfamily Conoidea),

seven species of Bivalvia, and seven species of Cepha-

lopoda, the latter probably pelagic. No representatives of

the family Architectonicidae were reported for the area in

the studies reviewed by these authors or any other study

until now. The new records of A. karsteni in the NDMP

provided as part of this study not only adds a species to the

malacological fauna reported for the Salas y Gomez and

Nazca Ridges, but also restores a species to Chile that has

been believed extinct from its jurisdictional waters since

23-17 Ma (Nielsen and Frassinetti, 2007; Nielsen and

Glodny, 2009; Finger et al., 2013).

Page 66

THE NAUTILUS, Vol. 134, No. 2

Figures 8-11. Architectonica karsteni sampled in Desventuradas islands (—25.4272°,—-81.8806°). 8-9. Dorsal, lateral and ventral

views of specimens 6928a and 6928b (scale bar = 1 cm). 10. Teleochonch and 11. protoconch (scale bar = Imm, SEM) sculpture of

SCBUCN 6928a. Arrows in 10 indicate whorl border sutures and the arrow in 11 shows the border of the protoconch.

The presence of A. karsteni in the seamounts of NDMP

may result from two alternative scenarios. The first is that

the sampled individuals could belong to relict populations

that persisted in the area since the Miocene. The sea-

mounts where the A. karsteni specimens were collected

have ages between 32 and 34 Ma (EarthRef.org, 2019)

Omalogyra fusca

Omalogyroidea

Omalogyra sp.

Architectonica perspectiva

Architectonicoidea

Architectonica karsteni

Cornirostra pellucida

Valvatcidea

Valvata piscinalis

Figure 12. Maximum-likelihood inferred phylogenetic re-

construction based on 580-bp alignment of partial COI se-

quences of species of Architectonicoidea (A. karsteni SCBUCN

7066, Accession GenBank # MN270389 and A. perspectiva -

FJ917269), Omalogyroidea (Omalogyra fusca - FJ917272,

Omalogyra sp. - FJ917273) and Valvatoidea (Valvata piscinalis -

FJ917267, Cornirostra pellucida - FJ917282). Only bootstrap

values above 90 are shown.

and likely hosted active reefs on their summits during the

Miocene, as indicated by fossil corals and gastropods

found on nearby seamounts (Menard, 1964; Gevorkyan

et al., 1987). After oceanographic changes occurred that

resulted in loss of populations across their geographic

range, the relict populations of A. karsteni could have

remained isolated without undergoing changes in shell

morphology, which would be consistent with evidence

suggesting that Architectonicidae of the Indo-Pacific is a

slowly evolving group (Bieler, 1993). Bieler based this

conclusion in part on the lack of morphological differ-

ences found between Indo-Pacific and Atlantic species

despite the genetic flow between them ceasing with the

closure of the Isthmus of Panama in the Pliocene (~3.5

Ma). It has been suggested that the Humboldt Current

System, with its characteristic cold and nutrient-rich

waters, could act as a barrier, at least, separating the

biota of this area from the South American coast

(Friedlander et al., 2016). Moreover, seamounts are also

known to generate particular circulation patterns (e.g.,

Taylor column, Taylor cone) that could contribute to the

retention of locally generated larvae (Rogers, 1994; 2018).

All these physical factors could contribute to the isolation

of the local fauna, resulting in the populations of sea-

mounts being repopulated with larvae generated within

the nearby seamount populations and under complete

isolation since 23 mya (Nielsen and Frassinetti, 2007). The

oceanographic changes registered since the Miocene

along the coast may not have affected the seamounts but

may have isolated the seamount populations of A. karsteni

from the continental coasts. If these isolated populations

C.M. Asorey et al., 2020

0.3

ew yy NSM Ope m

ce et A OD ts

Page 67

Pe Deion

: " J 5 m4 SP.

sons Archhectonicidae sp.

~ Architectonicidae sp.

Archikectonici e Sp.

Architectonicidae $

ee Architectonic

~ Architectonic i.

oe Are nectonicidae s sD.

~ Architectonicidae $p.

i Architectonicidae SP.

~ Architectonicidae sp.

pot itectonicidae sp.

; Architectonicidae SP.

~ Architectonicidae sp.

Archtectonicidae sp. 2

~ Architectonicidae sp.

Architectonicidae sp.

Architectonicidae $p.

pp ee $p.

~~ Architectonicidae sp.

Architectonicidae $p.

Architectonicidae <p. MH:

Architectonicidae sp. H2

~~» Architectonicidae sp. H1

~ Architectonicidae so. H

Arthitectonica maxi,

» Architectonicidae Sp. H27

Architectonicidae sp. Hz

Architectonicidae sp. H:

Architectonica an

Cut * € « . * © © @ VU

Acad ie cdl al a

OOMAWWOOD-\D00d, Oreos

rrxrxrrxr

E ,

Architectonicidae $p. H

- Architectonicidae sp

Architectonicidae sp

Architectonicigac | +P

Architectonica karste

Architectonicidae sp. H2

Architectonicidae sp. H37

~~ Architectonicidae sp. Hi 3

- Architectonicidae sp. H1

» Psiaxis radiatus

Figure 13. Maximum-likelihood inferred phylogenetic reconstruction based on 415 -bp alignment of partial 16S rRNA 16S sequences

of 50 haplotypes of Architectonicidae sp (MH557974 to MH558022), Architectonica maxima (KP252986), A. perspectiva (FJ9117251),

A. karsteni (MH270388) and Psilaxis radiatus (AY081999).

continued to evolve genetically with little changes in shell

morphology, A. karsteni found on the NDMP seamounts

could be a cryptic (and possibly sibling) species of pop-

ulations currently living on the continental shelf of the

Pacific coast of Central America, as documented for

several sacoglossan sea slugs species (Carmona et al.,

2011). The fact that A. karsteni has not been sampled

from other seamounts is not attributed to the mesh size

used in other studies, since gastropod species with similar

or even smaller sizes have been reported (e.g., Ptycho-

syrinx naskensis Sysoev and Ivanov, 1985). Neither is it

likely related to differences in depth of the seamounts

sampled, because the depths of the seamounts sampled

during the CIMAR 22 (Table 1) were in the same range as

previous expeditions (Parin et al., 1997). Although we still

cannot rule out insufficient sampling effort, the absence of

A. karsteni in other seamounts may have been due to the

existence of differences in the oceanographic conditions

and subsurface marine currents that may affect the

subsistence of this species directly, or indirectly through

effects on their cnidarian preys.

In the second scenario, the sampled population could

be the result of colonization of these seamounts after the

extinction of A. karsteni from this latitude during the

Miocene. Architectonicids are known to produce tele-

planic larvae able to drift in near-surface currents

(Scheltema, 1968, 1971: Scheltema and Williams, 1983)

and to delay metamorphosis; thus, their larvae can dis-

perse over great distances (1,000’s of km under suitable

current conditions). In this scenario, the sampled pop-

ulations would represent recolonization events of this

_region. Gene flow could exist between populations of the

NDMP seamounts and the continental shelf of the Pacific

coast of Central America and both populations would be

thus be part of a metapopulation.

Addressing the history of these populations would thus

require appropriate sampling methods to clarify the entire

range of the species and to obtain samples suitable for

detailed morphological and genetic analysis. Although the

systematic position, based on anatomical characters, and

complicated taxonomic history of Architectonicidae hans

been discussed by Haszprunar (1985, 1988) and Bieler

Page 68

(1988, 1992), little attention has been paid to the genetic

differences that may exist within and among Archi-

tectonicidae species. Therefore, few sequences are

available for addressing phylogenetic relationships within

Architectonicidae and to assess issues of historic and

modern population connectivity. Not enough genetic data

are available, and we did not have access to sufficient

samples of A. karsteni to determine whether the sampled

populations represent relict populations, cryptic Species,

or a recent colonization of modern A. karsteni. Accord-

ingly, we provide barcode data from one of our specimens

as an aid to future studies. To date, only 63 partial gene

sequences are available in GenBank, 50 of which are larval

16S rDNA sequences from specimens that were not

identified below family. Interestingly, only two COI se-

quences are available for Architectonicidae, despite this

genetic marker being widely used for DNA barcoding of

marine species (Bowen et al., 2014). The barcode data

provided here were used to confirm the phylogenetic

placement of this species relative to Architectonicidae

with published 16S and COI sequences. Although the

COI sequences A. perspectiva (FJ917269) and P. lutea

(AY296843) had a similar percentage of mutations com-

pared with A. karsteni, P. lutea presents a higher number

(6) of non-synonymous mutations across a similar number

of base pairs (623 vs 573 bp). In addition, the 165 rRNA

data supports the position of our A. karsteni specimen as

belonging to the genus Architectonica, of which A. per-

spectiva is the type species. Thus, this genetic data from

the NDMP specimens are consistent with our classifica-

tion of A. karsteni based on the morphological charac-

teristics. To further elucidate the taxonomic status of this

NDMP population and to assess potential crypsis, future

studies should address a more representative genetic

sampling of the group, including specimens throughout

the entire distributional area.

CONCLUSIONS

Until now, the malacofauna of Salas y Gomez and Nazca

Ridge seamounts is considered to have a high affinity with

the Indo-Pacific fauna (Parin et al., 1997). However, a

recently described species, Atrimitra isolata, seems to

have morphologic affinities with species from the

southeast Pacific coast (Sellanes et al., 2019). Similarly, we

report a species that was present at the coasts of conti-

nental Chile during the Miocene. This new record of A.

karsteni, together with the discovery of the above men-

tioned new species in NDMP, highlights the need for

more studies of the region, which not only focus on

biodiversity but also on the phylogenetic relationships

between them and the fauna of surrounding areas.

ACKNOWLEDGMENTS

For their assistance at sea, we would like to thank the

Captain and crew of R/V caso DE HORNOS of the Chilean

Navy, and the scientific personnel participating in the

THE NAUTILUS, Vol. 134, No. 2

CIMAR 22 cruise. Special thanks to Jan M. Tapia and

Jorge Avilés for their help during collection, handling and

curation of the specimens. We are grateful to Dr. Matthias

Gorny from OCEANA who piloted the ROV that obtained

the images of the habitat at the seamounts surveyed in this

study. Thanks to Jan M. Tapia for the ROV photos. CMA

thanks Dr. Rubén J. Diaz for his unconditional support

and for encouraging her to continue in the race. Sug-

gestions by Sven Nielsen and an anonymous reviewer

greatly helped to improve the manuscript. Funding was

provided by grants CONA C22 16-09, FONDECYT

1181153 and FONDEQUIP EQM150109 to JS; New

Hampshire-INBRE through an Institutional Develop-

ment Award (IDeA), P20GM103506, from the National

Institute of General Medical Sciences of the National

Institutes of Health; and Millennium Nucleus ESMOI

(NC120030).

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THE NAUTILUS 134(2):71-88, 2020

Page 71

A history of eastern Pacific marine heterobranch research

Hans Bertsch!

192 Imperial Beach Blvd., Unit A

Imperial Beach, CA 91932

[email protected]

“The Mollusks whose history and characters it is the pur-

pose of the present work to illustrate, form an attractive

group of the class Gasteropoda, until lately little noticed,

and supposed to be of small extent, but which modern re-

searches have brought into more prominent importance.”

Joshua Alder and Albany Hancock, 1845,

A Monograph of the British Nudibranchiate Molluscs

We live in one interconnected global ecosystem, from the

butterflies in the Amazon to the polar bears on the Arctic

ice. Because of radical anthropogenic activities, today the

tropical rain forest is burning and the polar ice caps are

melting. Earth’s health is in danger. The need for good

science, historical perspectives, and rational decisions is

even more imperative. Contributions to our knowledge of

the biodiversity in any faunal region form a significantly

useful aspect in our search for understanding and pre-

serving life on earth.

By its nature, in terms of both the observers and the

observed, science is an international endeavor (Gosliner,

Cervera, and Ghiselin, 2008). Science is without borders.

This is especially demonstrated by the history of “opis-

thobranch” research in the northeastern Pacific. From

Alaska to Peru, these animals have distributions spanning

multiple countries on both sides of the northern Pacific.

The investigators have been equally international. For

instance, Johann Eschscholtz, from modern Estonia,

participated in two circumglobal expeditions in the early

19% century, collecting in regions that flew different flags

than today. From Spanish and Mexican California, and

Russian Alaska, he named a nightshade plant, a tene-

brionid beetle, two salamanders, a sand dollar, and two

nudibranchs. The Danish physician Ludwig Sophus

Rudolph Bergh named a number of Alaskan nudibranch

species based on specimens collected by the U.S. mala-

cologists William Healey Dall and William Simpson, in-

cluding the still-valid species of nudibranch Dendronotus

dalli, which he described only from the pharyngeal bulb of

an unknown animal! Today such international cooperation

! Research Associate in Malacology, Los Angeles County Natural History Museum

includes co-authorships, sharing of specimens, and joint

research expeditions. Especially notable are DNA phy-

logenies involving collaborating researchers from multiple

countries.

Science builds on both the research results and the

investigative methods and publication styles of previous

generations. Compendia and monographs of taxonomic or

geographic groups were, and are, the technical equiva-

lents of the modern field guides. During the 18" and 19%

centuries, numerous volumes on conchology were pub-

lished, highlighted by the works of British natural history

aficionados such as the Rev. John Lightfoot (1786), the

Sowerbys I and II (1821-1875), Lovell Augustus Reeve

(1841-1860), and the Rev. Philip Pearsall Carpenter

(1855-1872). These guides to almost-random geographic

areas, were based on shell collections in British cabinets.

Apparently dead sea shells are more attractive and col-

lectible than pickled sea slugs!

The first comprehensive monographs on the nudi-

branch fauna of a region (with color illustrations of living

animals) was Joshua Alder’s and Albany Hancock’s

magnificent series on their own British Isles (1845-1855).

Later compendia were a mix of national and international

efforts. Especially significant (among many others) were

Bergh’s (1905) German report on the stgoca Expedition

to the Netherlands’ East Indies Colonies, Charles Norton

Edgecombe Eliot’s studies in the Indian Ocean

(1902-1916), Kikutaro Baba’s (1949, 1955) descriptions of

specimens collected by His Majesty the Emperor of Ja-

pan, in Sagami Bay, and Jean Risbec’s (1956) work on

Vietnamese species.

Myra Keen’s second edition of Sea Shells of Tropical

West America (1971) included a section on nudibranchs.

Based on a species list compiled by H. Bertsch, Wesley

Farmer and Steven Long, the overview was written by

James Lance. It included brief descriptions of 72 species,

notes on their habitats and distribution, and four plates of

color photographs of the living animals.

In 1976, Thomas E. Thompson and Gregory H. Brown

published a guide to the British opisthobranch mollusks,

with detailed drawings and anatomical and life history

information. Schmekel and Portmann’s (1982) guide to

Mediterranean opisthobranchs included magnificent full-

Page 72

color paintings of each species by Iona Richter, along with

comprehensive anatomical, biogeographic, and taxonomic

data.

Field guides have played an important role in expanding

access to natural history information and identification of

species’ groups for “citizen scientists.” First popularized for

birds (e.g., Peterson’s Identification System of the 1930s),

these works now cover almost all aspects of the biological,

geological, and chemical realms on and off the planet. Of

course, the nudibranchs began to receive attention.

The first field guides, illustrated completely by full-

color photographs of living opisthobranchs, appeared

within about a year’s span. McDonald and Nybakken

(1980) published a guide to the nudibranchs of California

(with 112 species). They included a dichotomous key for

identification of the organisms and an aquarium photo of

each species. Dave Behrens (1980), in the first edition of

his book, published a comprehensive guide to all the

known 162 heterobranch species in the northeast Pacific,

from Alaska to the southern tip of the Baja California

peninsula. Bertsch and Johnson (1981) documented 78

species from the Hawaiian Islands, often presenting

multiple in situ photographs of an animal’s life history. For

the far western Pacific, John Orr (1981) published

aquarium photos of some 50 species of Hong Kong nu-

dibranchs, representing just a part of what he considered

to be a far more extensive fauna.

Since these works, and with the increased popularity of

underwater macro-photography by scuba divers, nu-

merous nudibranch field guides have appeared in multiple

languages for various parts of the world’s oceans: e.g.,

Arctic and Russian Seas (Martynov and Korshunova,

2011), the Indo-Pacific (Gosliner, Behrens, and Valdés,

2018), Korea (Koh, 2006), Bali and Indonesia (Tonozuka,

2003), Australia’s Great Barrier Reef (Marshall and

Willan, 1999), Mexico (Hermosillo et al., 2006), the

Caribbean (Valdés et al., 2006), and Brazil (Garcia-Garcia

et al., 2008). The list keeps expanding!

Multiple conferences dedicated to sea slugs have been

organized (Malaquias et al., 2011). Since its inception, the

Western Society of Malacologists has presented near-

annual opisthobranch symposia at its meetings, with in-

ternational participation (Figures 1-3). The International

Workshop of Opisthobranchs, now the International

Heterobranch Workshop (!) has been held at various sites

around the world (Figure 4).

With the wealth of information accessible electronically,

there are highly useful web sites dedicated to sea slugs, most

notably Bill Rudman’s Sea Slug Forum (not currently active,

but archives are available at www.seaslugforum.net ), and

Mike Miller’s Slug Site (now in its 21° year, found at

www.slugsite.tierranet.com ), with ongoing weekly post-

ings. Especially significant is Gary McDonald’s compre-

hensive Bibliographia Nudibranchia. Numerous underwater

photographers post brilliant photographs on their personal

sites. The change from film to digital cameras has helped

greatly to revolutionize nudibranch imaging.

Indeed, today—as Alder and Hancock observed nearly

two centuries ago—sea slugs have been “brought into

THE NAUTILUS, Vol. 134, No. 2

Figure 1. Eveline Marcus (left) and Louise Schmekel,

Monterey, California, July 1986. (Photo by Hans Bertsch)

more prominent importance” than even those prescient

investigators would have imagined.

This work is a human and scientific history, describing

the individual scientists and the development of our

Figure 2. Slug Talk. Presentation announcement of opis-

thobranch workshop, Seattle, Washington, August 2006.

(Drawing by Jan Kocian)

H. Bertsch, 2020

Page 73

Figure 3. Opisthobranch workshop participants, joint meeting of the Western Society of Malacologists (WSM) and the American

Malacological Society (AMS), Seattle, August 2006.

understanding of the marine heterobranch fauna from

the eastern Pacific, from the southern limit of the Panamic

Province to the Arctic shores of Alaska. Although nu-

merous, the terrestrial species of Heterobranchia (land

snails and slugs) are not included. To establish a wider

context, various early voyages of exploration along the

Pacific coast are mentioned, along with broader, non-

heterobranch molluscan studies. It should be noted that

many of the pioneering naturalists published on a wide

variety of disparate taxa across phyla and even kingdoms

(Bertsch, 2015). Recent taxonomic changes based on

DNA analyses have completely revised the traditional

classification schemes. Although Opisthobranchia is no

longer considered a valid monophyletic taxon, the term is

used throughout this work in its historical sense.

138

“A number of times we were asked, Why do you do this

thing, this picking up and pickling of little animals? Finally

we learned to know why we did these things. The animals were

very beautiful. Here was life from which we borrowed life and

excitement. In other words, we did these things because it was

pleasant to do them.... Here was no service to society, no

naming of unknown animals, but rather—we simply liked it.”

John Steinbeck and E. F. Ricketts, 1941,

Sea of Cortez

Based on the publications of investigators, one can identify

seven historical periods of “opisthobranch” research in the

eastern Pacific. Until the recent explosion of nudibranch

interest and researchers, most of the periods are represented

each by only a handful of persons. Authorship of a

publication is only the beginning of a historical perspective.

Who were these researchers? What were their meander-

ings? What was the scope of their scientific investigations?

The international character of the research has been a

constant. Today’s known eastern Pacific fauna consists of

species with type localities around the world, described by

researchers of multiple nationalities. This chapter describes

key aspects of these investigators’ lives and their endeavors.

During these periods there have been significant de-

velopments in our knowledge of the taxonomy and natural

history of the marine heterobranchs from this region.

There has been a dramatic change in the numbers of

species named (and the taxa to which they belong) before

and after 1961. Before 1961, the Nudipleura constituted

only 60% of the known heterobranch species. Today,

however, they make up 75% of all known marine het-

erobranch species in the eastern Pacific. In the 200 years

from 1761-1960, 104 species of Nudipleura were named,

contrasting with 72 species of the non-nudipleuran het-

erobranchs. During the 60-year span from 1961-2019 the

numbers of nudipleura species named increased to 168

but decreased to 25 for the non-nudipleuran hetero-

branchs (Figure 5). The total numbers of species and the

average numbers named per year showed several pat-

terns. The average number of nudibranchs named in-

creased dramatically from 0.5 to over 2.5 species named

per year before and after 1961. However, the yearly av-

erage of species named among all the other Hetero-

branchia (many of these are the shelled forms) remained

the same, less than 0.5 (Figure 6). Looking at each of

the seven periods described below, one sees a near-

constant annual number of non-nudipleuran heterobranchs

named, but a significant increase in the numbers of species of

Page 74

THE NAUTILUS, Vol. 134, No. 2

Figure 4. Participants at the 4 International Workshop on Opisthobranchs, meeting of the WSM, University of California, Santa

Cruz, June 2012. }

Nudipleura named per year (Figure 7). Because the periods

vary in length, the average named per year is more indicative

of the research eftorts and shows more precisely the pro-

nounced increase in the naming of Nudipleura species

(Figure 8).

1. Pre-1860: From Indigenous Peoples and Foreign

Visitors to Gould

Indigenous people living on the Pacific coast of North

America have been well acquainted with mollusks, in-

cluding Heterobranchia, for centuries. Mollusks are

dominant components of midden mounds along the

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shores of the eastern Pacific (e.g., Tellez-Duarte et al.,

2001, upper Gulf of California; Glassow, 2010, Channel

Islands; and Trant et al., 2016, British Columbia). Nu-

merous shelled gastropods have been found in these

“trash dumps,” but no marine heterobranchs have been

recorded from any of them. Therefore, any knowledge,

use, or consumption of sea slugs by indigenous nations can

only be documented by ethnohistorical methods. The oft-

cited report of Tritonia tetraquetra being named “Tochui,”

and consumed by the Kuril Island people (Pallas, 1788) is

probably based on a linguistic misinterpretation. The similar-

sounding Ainu word togoi, means invertebrates or mollusks

in general, which were consumed, but not specifically the

rin ANE

1961-2019

Figure 5. Numbers of pre- and post-1961 descriptions of eastern Pacific Heterobranchia species. Orange: Nudipleura. Blue: Non-

Nudipleura Heterobranchia.

H. Bertsch, 2020

Yearly Number of Species Named

fond

taverns

1761-1

960 1961-2019

Figure 6. Annual number of eastern Pacific Heterobranchia

species named pre- and post-1961. Colors as in Figure 5.

deep-water tritoniid nudibranch (Martynov, pers. comm., 11

September 2011).

For centuries, the Comcaac (Seri) of Sonora have been

gathering mollusks for food, games, and decorative and

medicinal uses along the eastern shores of the Gulf of

California. They knew about and used sea slugs, even

giving common names to four species. This rich ethno-

historical cultural knowledge has been passed on to the

present generation (Marlett, 2014: 168-171). Bulla

gouldiana is called cacaapxon, “what fattens some-

thing.” Living animals of B. gouldiana were played with

by children who shot them like marbles, and the sticky

animal would sometimes adhere to the target. Empty

shells were strung in necklaces or used as dangling ear

ornaments (Bertsch and Marlett, 2011). Found on

shallow sand flats, Navanax inermis was aptly named

hant iti queemij, “what moves slowly on land.” Aplysia

californica, occasionally used as bait, was given the

name hatx cdcazoj. The etymology is unclear, but hatx

refers to rump or buttocks. The color purple was even

named “the ink of hatx cdcazoj.” The blood-colored ink

of Aplysia caused precautionary warnings that preg-

nant or menstruating women not touch it. Finally,

Berthellina ilisima is named xepenozaah, “sun in the

sea.” Imagine rolling rocks in the intertidal zone under

the glaringly hot Sonoran desert sun and finding this

orange blob!

Total Number of Species Named

Page 75

With the exception of Eschscholtz, prior to 1860,

marine heterobranch species now known to occur in the

eastern Pacific were named scientifically from specimens

collected from other regions, or by investigators who were

not working in this region. For instance, Aeolidia papillosa

(Linnaeus, 1761) was first reported from the northeastern

Atlantic, Dolabella auricularia (Lightfoot, 1786) was

based on an internal shell collected in the Indo-Pacific,

and the type material of the previously mentioned Tri-

tonia tetraquetra (Pallas, 1788) was collected from the

Kuril Islands, in the northwest Pacific.

The publication of Eolidia (now Fiona) pinnata and

Cavolina (now Hermissenda) crassicornis by Eschscholtz

in 1831 first named a nudibranch species from a type

locality (Sitka, Alaska) in the eastern Pacific (Figure 9).

Johann Friedrich von Eschscholtz (1793-1831) served as

surgeon and naturalist on two circumglobal Russian ex-

peditions commanded by Otto von Kutzebue, on board the

RURIK (1815-1818) and the PREDPRIAETIE (1823-1826). His

zoological results of these journeys described species across

a wide assortment of taxa. In addition to the previously

mentioned species, he named the marine turtle Lep-

idochelys olivacea (Eschscholtz, 1829) based on specimens

from Manila and Sumatra, and King Kamehameha’s but-

terfly Vanessa tameamea (Eschscholtz, 1821) from Hawaii.

After his voyages, Eschscholtz returned to teaching full-

time as Professor of Anatomy at the University of Dupat.

During the first half of the nineteenth century, other

sailing expeditions brought additional specimens from

around the world back to Europe to be named. For ex-

ample, the French voyage of the ASTROLABE (1826-1829),

commanded by M. J. Durant d’Urville, brought back

shells of tropical aplysiids that were named by Quoy and

Gaimard (1832). These military and scientific expeditions

spurred the United States to finally launch its own national

exploring survey. Although the planning stages were

plagued by personal jealousies, and political and financial

obstacles, a flotilla of six vessels finally departed Norfolk,

Virginia, on 18 August 1838, under the command of

Charles Wilkes. Over the span of four years and 87,780

miles, this United States Exploring Expedition (U.S.E.E.)

crisscrossed, surveyed and dredged the oceans, and even

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Historical Time Periods

Figure 7. Numbers of eastern Pacific Heterobranchia species named by historical period. Colors as in Figure 5.

Page 76

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THE NAUTILUS, Vol. 134, No. 2

4 5 6 7

Historical Time Periods

Figure 8. Annual numbers of eastern Pacific Heterobranchia species named per historical period. Colors as in Figure 5.

collected on land and in rivers. Two vessels were lost at

sea, and two were deemed unseaworthy. Only the vinc-

ENNES and the PORPOISE sailed the entire voyage. The

description of the marine mollusks collected during this

expedition was entrusted to Augustus Addison Gould.

Dr. Gould (1805-1866) was a Boston physician, in-

strumental in the founding and success of the Boston

Society of Natural History. As a young college student, he

began a lifelong interest in natural history. While practicing

as a physician, he spent most of his spare time studying and

describing mollusk species. Because of his publications (see

Johnson, 1964), especially Report on the Invertebrates of

Massachusetts (1841), he was chosen to write the mollusk

report of Wilkes’ expedition. His description of the nudi-

branch Melibe leonina (Gould, 1852) was the first de-

scription by an American of a marine heterobranch

collected in the eastern Pacific. The type had been dredged

at Port Discovery, Puget Sound, by Mr. Dyer of the

U.S.E.E. Subsequently Gould (1853, 1855) named four

cephalaspideans, two collected by Colonel Ezekiel Jewett

at Santa Barbara (Acteocina cerealis and A. culcitella), and

two from San Diego (A. inculta and Haminoea vesicula)

collected by William Phipps Blake. Jewett was an ac-

complished private collector; he had spent ten weeks in

Panama, then journeyed to California, collecting along the

coastline from San Francisco to Ventura. Blake had arrived

in California finishing a reconnaissance survey for a railroad

route across the southwestern United States.

A few years later, Gould’s correspondent and colleague,

the English-Canadian Presbyterian minister Philip Pear-

sall Carpenter (1819-1877) named five species of eastern

Pacific shelled slugs from Mazatlan, southern California,

and Puget Sound (Palmer, 1958). He studied additional

material from the collections by Jewett and others that

Gould had used. Carpenter’s original descriptions of some

species were rather terse, e.g., Volvulella cylindrica was

“like a grain of rice, pointed at one end,” and Rictaxis

punctocaelatus was “Small: grooved with rows of dots:

pillar twisted as in Bullina.” In later publications, he did

present more expansive and detailed descriptions.

Prior to 1860 with the exception of Eschscholtz, het-

erobranchs now known to occur in the eastern Pacific

were described from specimens collected in other marine

provinces, or by investigators who were not working in this

region. This was about to change.

9. 1860-1875: Pioneering Intertidal Naturalists

The second period of eastern Pacific opisthobranch re-

search encompasses the work of three men who were the

first scientists actually to live in this region and to name

heterobranch species which they had collected.

At the beginning of the century, Eschscholtz had ar-

rived at the shores of western North America by sailing

vessel and then returned to his native Estonia to even-

tually publish his findings in the German narratives of the

Kotzebue expeditions. In contrast, James Graham Cooper

(1830-1902) traveled by boat and horseback to the U.S.

Pacific coast and then stayed there, publishing his ob-

servations in English in the Proceedings of the California

Academy of Sciences (of which he was an early member),

and other U.S. journals and scientific government reports.

Both men were accomplished field biologists, by land and

sea, and skilled writers, describing a diversity of marine

invertebrates, terrestrial fauna, and flora. Before settling

in central California to earn a living in medicine, Cooper

served as a contract surgeon and naturalist on railroad

surveys and military expeditions, traversing the continent,

exploring both the Atlantic and Pacific coasts and the

western deserts and mountains. He was the pioneer of

California nudibranch research, being the first to collect

and describe species from this coastline (Figure 10; Coan,

1982).

Upon graduation from the College of Physicians and

Surgeons in 1851, the young Cooper spent two years

practicing medicine at New York City Hospital. He was

then appointed physician and naturalist for the 1853-1855

Railroad Survey Expedition (under the command of

Captain George B. McClellan, who in 1862 led the Union

troops at Antietam) in Washington Territory. When fin-

ished, Cooper returned to New York, again by boat,

crossing the Isthmus of Panama. He spent the next five

years in New York and Washington, D.C., traveling the

east coast between New England and Florida, traversing

H. Bertsch, 2020 | | Page 77

Figure 9. Original illustrations of the first two nudibranch species named from the eastern Pacific, Eolidia (now Fiona) pinnata and

Cavolina (now Hermissenda) crassicornis. (Eschscholtz, 1831: Plate XIX, figs. 1 and 2

Page 78

Eugene Coan

Figure 10. Book cover of James Graham Cooper biography.

(Coan, 1982)

the U.S. to Wyoming Territory on the ill-fated 1857 Wagon

Road Expedition, and doing research in the major east coast

museums. He renewed his family’s earlier acquaintance with

Spencer Fullerton Baird, the first Curator of the United States

National Museum (USNM). It was Baird who recommended

him to participate in the 1860 Military Expedition to the West

as surgeon and naturalist. This expedition crossed the Rockies

through Montana, ending at Ft. Vancouver. From there he

went by steamer to San Francisco and then was posted for five

months at Fort Mojave, Arizona, on the east bank of the

Colorado River. Later he named a tortoise and bird he had

collected in the high desert region. When he returned to San

Francisco via San Diego, he collected along the coast and the

offshore islands. Now firmly ensconced in California, he was

hired by Josiah Dwight Whitney as Zoologist of the California

Geological Survey, collecting birds, mammals, fossils, and

marine organisms throughout the state. The last 40+ years of

his life he devoted to medicine, his family, field work, writing

and publishing, and serving the nascent California of Sciences

in a variety of curatorial and directorial roles.

Dr. Cooper had wide-ranging interests, from geology

and paleontology, to phytogeography and_ ethnology.

THE NAUTILUS Vol 1844No..2

Although the majority of his publications were on con-

chology, he also published papers on mammals (see

Taylor, 1919) and birds (see Emerson, 1899). His con-

tributions to ornithology were so impressive that when a

group of bird enthusiasts organized a study group in 1893,

they named it the Cooper Ornithological Club in his

honor. In addition to 10 species of bivalves and 89 species

of gastropods (E. Coan, pers. comm., December 2019),

Cooper named two species of brachiopods, one insect,

nine fish, two reptiles, four birds, and a subspecies of

mammal. His etymological explanations are sometimes

whimsical. He named Lucy’s Warbler Vermivora luciae in

honor of S. F. Baird’s daughter, whose “presence, like the

bird’s, would go far to make a garden of the desert.” The

desert tortoise Gopherus agassizii, which he considered

“the emblem of slowness,” he named in honor of Har-

vard’s anti-Darwinian professor Louis Agassiz! In naming

nudibranchs, he used no patronyms, but dedicated species

to a collecting location or a distinctive morphological

feature (e.g., sandiegensis and iodinea). Cooper’s 1863

paper described 14 species of nudibranchs (12 are still

recognized as valid today) which he had collected from the

coast and islands of southern and central California.

Robert E.C. Stearns (1827-1909) went back and forth

across the U.S. during his career. He worked as a pay-

master for copper mines in Michigan, then moved to

California in 1858 as editor of the weekly Pacific Meth-

odist. Along with the Unitarian minister Thomas Starr

King, his efforts significantly influenced the voters to

approve California’s statehood entry as a Union, non-slave

state. He was a Deputy Clerk of the California Supreme

Court, searched for mollusks in southwest Florida with

William Stimpson and Ezekiel Jewett, served as secretary

of the fledgling University of California, and was

appointed Assistant Curator of Mollusks at the United

States National Museum (USNM) by S. F. Baird, where

he worked until his death. Stearns published over 100

papers on “conchology,” several dozen on various forestry

and ethnology topics, and introduced species (Stearns,

1911). He named numerous molluscan species, including

the tropical eastern Pacific Conus dalli in honor of his boss

at the National Museum, William H. Dall. He named just

two heterobranch species, the common white-on-white

Tritonia festiva and the shelled Acteon traskii, the only

extant sea slug originally named from fossil material.

William More Gabb (1839-1878) served as the Pale-

ontologist for J]. Whitney’s California Geological Survey.

He described a number of marine shells that had been

collected by J. G. Cooper during that Survey, including

the umbraculid Tylodina fungina. His description was

based on “a single specimen, fresh, although without the

animal,” from Santa Barbara Island.

3. 1875-1900: L.S.R. Bergh

Worldwide opisthobranch research during this period was

dominated by one man, the prolific Danish physician

Ludwig Sophus Rudolph Bergh (1824-1909). Dr. Bergh

H. Bertsch, 2020

worked as a medical doctor for 50 years in several

Copenhagen hospitals. He specialized in the diagnosis,

prevention and treatment of sexually transmitted diseases.

When not working in medicine, he examined 1000s of

specimens and published over 90 articles and monographs

of sea slugs from around the world. As an anatomist he

emphasized the comparative morphology of the nervous

and reproductive systems and the radula in classifying

nudibranchs and their related taxa. He described more

than 500 species of sea slugs from around the world, but

only 18 valid species from the eastern Pacific. Of these, 13

had type localities in the eastern Pacific, based on spec-

imens dredged by the U.S. Fish Commission steamer

ALBATROSS (Elysia diomedea), or sent to him by William H.

Dall (Felimida dalli). One recently “re-discovered” spe-

cies, Akiodoris lutescens, was collected by Dall from the

low intertidal at Nazan Bay, Atka Island in the Aleutians;

the site lies just barely within the eastern Pacific, at

— -§2.232° N; 174.1726° W. Bergh noted, “The fauna of the

North Pacific in general has been but little explored. The

number of the so-called Nudibranchiate Gasteropod [sic]

Mollusca found in this region up to this time is rather

small...and the number of forms is much smaller than that

which is known from the North Atlantic in the same

latitudes. There does not, however, seem to be any reason

for a smaller number in the Pacific than in the Atlantic”

(Bergh, 1879). Researchers from California and Canada in

the early twentieth century proved his comments correct.

Upon Bergh’s death, Dall (1909) wrote that he “was

most genial and agreeable in manner, ever ready to help

younger students or serve as cicerone to foreign col-

leagues.... [A] staunch friend.”

4, 1901-1925: Canada and California

This period is distinguished from previous years by a group

of researchers who spent significant periods of time living

and collecting on the west coast, from California to Canada.

By far the most emphatic proponent of opisthobranch

research was Frank Mace MacFarland (1869-1951). He

was born in Centralia, Illinois, and after receiving his

bachelor’s degree he was hired as a professor of biology and

geology at Olivet College in Michigan. A few years later, the

ichthyologist David Starr Jordan hired him as an instructor

in histology at Stanford University. While teaching, he

earned his master’s degree there, and then a Ph.D. in

Germany from the University of Wiirzburg. Returning to

Stanford, he advanced to Professor of Histology. Mean-

while, he was instrumental in the founding of Hopkins

Marine Station in Pacific Grove, serving as co-director from

1915-1917. MacFarland retired from Stanford in 1934 and

was elected President of California Academy of Sciences, a

post he filled until 1946. He had met his wife, Olive

Knowles Hornbrook (1872-1962) in Indiana on his way to

Germany. She was an accomplished zoologist and a gifted

artist, producing meticulous drawings that accompanied his

publications. In the introduction to MacFarland’s post-

humous 1966 opus, then-President of California Academy

of Sciences, Robert C. Miller wrote simply, “|He] was one

Page 79

of the kindest and friendliest of men. He radiated

cheerfulness and goodwill.”

During the first quarter of the 20% century, MacFar-

land described 18 species of nudibranchs, mainly from

intertidal regions around Monterey Bay and Pacific Grove

(Figure 11). His description in 1925 of the pungently

aromatic Acanthodoris lutea was based on two specimens,

one of which had been collected by Dr. Myrtle Elizabeth

Johnson at Cayucos, in San Luis Obispo County. She and

Harry James Snook (1927) published Seashore Animals of

the Pacific Coast, the first comprehensive guide to the

common seashore animals of the west coast of the U.S.

Although their book included color drawings of 20 nu-

dibranchs, neither they nor MacFarland ever published a

color painting of this vivid, bright orange species.

The importance of MacFarland’s contributions to our

knowledge of eastern Pacific heterobranchs, along with

his enthusiasm and inspiration to others, cannot be over-

emphasized.

The Englishman Charles H. O’Donoghue (1885-1961)

was a professor at the University of Manitoba and Director

of the Marine Biological Station at Nanaimo on Vancouver

Island. He returned to the British Isles in 1928, teaching

at Edinburgh and Reading University. In a series of papers

between 1921-1927, he described the nudibranch fauna

of the Vancouver Island region, naming nine new species.

He reported on a collection of 28 species of nudibranchs

collected by W.A. Hilton and students from Laguna

Beach. Hilton was the director of the Laguna Marine

Laboratory (Pomona College, Claremont) and encour-

aged nudibranch research by his students (see Bacon,

1913). He was honored with O’Donoghue’s Phidiana

hiltoni.

Theodore Dru Cockerell (1866-1948) was also born in

England but had to leave for health reasons. He spent

most of his professional life at various museums and

universities in Jamaica, New Mexico, and Colorado, and

became a U.S. citizen. Primarily an entomologist, he was a

prolific namer of living and fossil insects, mollusks and

plants, and other taxa. He named over 6,000 species and

genera of Hymenoptera, including a remarkable 34

million year-old wasp found embedded in amber from

Colorado’s late Eocene Florissant Formation. He and his

second wife, Wilmatte Porter Cockerell, traveled widely,

even crossing Russia on the Trans-Siberian Railroad. They

were in Japan during the Great Kantu Earthquake of

1923. This 7.9 magnitude quake devastated Tokyo and

Yokohama and generated a tsunami of 10 m which struck

the coast of Sagami Bay. Years later in this bay, Emperor

Hirohito collected the nudibranchs described, illustrated,

and named by Kikutaro Baba (1949, 1955). Cockerell’s

visits with his wife to tide pools in southern California

resulted in the collection of a number of new species. He

and MacFarland reciprocated patronyms. Cockerell also

named species in honor of his wife, J. G. Cooper, and R. E.

C. Stearns.

The peripatetic British ambassador, colonial commis-

sioner, and University Vice-Chancellor, Charles Norton

Edgecumbe Eliot (1862-1931), published numerous

Page 80

hLhCr™rts—COCOC

THE NAUTILUS, Vol. 134, No. 2

Figure 11. An original painting of Chromodoris porterae Cockerell, 1901, by Anna B. Nash, artist of the Hopkins Seaside Laboratory.

(MacFarland, 1905: Plt. XXVI)

descriptions of nudibranchs, especially from Antarctica

and the Indian Ocean. Cockerell and Eliot (1905) re-

ported on a collection of Californian nudibranchs,

resulting in five new species and a genus with authorship

cited as “Cockerell in...” (e.g., Anteaeolidiella chromo-

soma) or “MacFarland in....” (e.g., Dirona picta).

William Healey Dall (1845-1927) is a bit difficult to place

within one period, since his publications spanned decades,

from 1866 to (posthumously) 1938, and he interacted with

numerous researchers. He is considered here because he

named most of his heterobranch species (14 of 18) during

this time period. Like so many other workers up to this

period, his primary focus was not specifically on sea slugs.

For instance, he not only named a species of abalone

(Haliotis), but had one named in his honor. A decades-long

curator of mollusks at the USNM, Dall was a profligate

namer of genera and species, totaling (including the syn-

onyms) 5,302 molluscs and 125 non-molluscan inverte-

brates (Boss, Rosewater, and Ruhoff, 1968). This was a

tremendous amount of names to devise, but only 27 names

were used more than ten times. His most common pat-

ronym (used for 17 species) was stearnsii, honoring his

contemporaneous fellow mollusk curator at the USNM,

Robert Stearns. Dall also named the genus and species of

the barnacle Cryptolepas rachianecti, which lives only on

the California gray whale, annually migrating from Alaska

to the Pacific lagoons of Baja California Sur. Dall had made

a number of expeditions to Alaska, both before and after

the U.S. had purchased it from Russia.

Based on two pale green empty shell valves collected by

Charles R. Orcutt from Bahia Magdalena, Dall (1918)

named the “clam” Scintilla chloris. Since the late 19%

century, fossil shells of Juliidae had been considered mytilid

clams. However, Kawaguti and Baba (1959) found living

specimens of this group in Japan, among the green Cau-

lerpa alga. They described the animals correctly as bivalved

sacoglossans. Dall’s species is now Berthelinia chloris,

properly ensconced as a sacoglossan heterobranch. Some

years earlier Dall (1884) had named the southern California

“naked” clam Chlamydoconcha orcutti. The collector and

describer had unwittingly collaborated in a polar coinci-

dence: a bivalve slug and a slug-like bivalve! Orcutt

(1864-1929) was a San Diego cactologist and malacologist,

instrumental in founding the San Diego Natural History

Museum. He traveled extensively throughout northern

Baja California and elsewhere (DuShane, 1971), eventually

dying in Haiti from malaria.

5. 1926-1960: An Inter-Period

Eastern Pacific opisthobranch research endured a slow-

down of activity during this period. Although Japanese

(Kikutaro Baba), French (Alice Pruvot-Fol) and Swedish

(Nils Odhner) authors were publishing major papers on

H. Bertsch, 2020

new species of opisthobranchs globally, only 11 species

were named from material that was originally found in the

eastern Pacific. MacFarland and/or O'Donoghue named

five of these, based on their earlier collections. Two

aplysiids, three shelled species, and one noteworthy nu-

dibranch constitute the rest. The nudibranch was a pat-

ronym, named by his colleague G. Dallas Hanna: “A few

minutes before Dr. F.M. MacFarland collapsed on

February 21, 1951, he discussed with me the generic

position of a rather remarkable species of nudibranch....

He unquestionably would have described this animal in

his very thorough manner had fate permitted. As a poor

substitute, I will endeavor to place it on record and it

seems fitting that it be named for him,” Platydoris

macfarlandi Hanna, 1951.

Several other regional publications on the natural

history and biodiversity of sea slugs deserve mention.

Costello (1938) described and illustrated the egg masses

and reproductive periodicity of 22 species of nudibranchs

in the Monterey Bay region, and Steinberg (1954) pub-

lished a dichotomous key identifying 50 of California’s

more common opisthobranchs. Sea of Cortez: A Leisurely

Journal of Travel and Research (Steinbeck and Ricketts,

1941) did not immediately garner the attention it de-

served since it was published on the 6" of December, the

day before Pearl Harbor was bombed by the Japanese,

which plunged the United States into the global war ef-

fort. Today, this book is acknowledged as the pioneering

research publication concerning the living marine inver-

tebrates of the Gulf of California. This collaboration

between a Nobelist in Literature, John Steinbeck

(1902-1968), and a Monterey Bay marine biologist,

Edward F. Ricketts (1897-1948) describes their six-week

expedition doing science, and the people they met and the

places they visited, as well as including a scientific cata-

logue of the specimens they observed or collected. In this

work they discussed the natural history and biogeography

of 14 species of heterobranchs, including a “large seal-

brown nudibranch” (possibly Cadlina luarna). They

correlated regional and seasonal temperature variations of

the waters of the Gulf with the co-occurrence of fauna

from the southern tropical regions of the Panamic

province and the northerly temperate California province,

being the first investigators to comment on the ecotonal

nature of the Cortezian province.

6. 1961-2000: Coming of Age

Possibly the surge in opisthobranch research in 1961 and

the founding of the molluscan journal The Veliger by Dr.

Rudolf Stohler was a synergistic coincidence. Numerous

articles on eastern Pacific heterobranchs have been

published within its pages. Between 1959-1961 resident

researchers Joan E. Steinberg and James R. Lance

published a series of papers in The Veliger updating the

nomenclature and known distribution of opisthobranchs

from the west coast of North America. Steinberg is now

retired, having spent her career as an award-winning

elementary and middle school teacher in San Francisco.

Page 81

Lance (1928-2006) lived for decades on Agate Street in

La Jolla, just blocks from his long-term intertidal col-

lecting area. He worked as a laboratory technician in the

laboratory of Dr. William Fenical at Scripps Institution of

Oceanography (SIO), tending algae and collecting in-

vertebrates for chemical studies in marine pharmacology.

Five species of nudibranchs and sacoglossans that he

described from the eastern Pacific are still considered

valid. 7

In a 1961 supplement to volume 3 of The Veliger, Ernst

Marcus described the anatomy and distribution of 50

species of opisthobranchs from California, from which he

named 11 new species (five are still considered valid). The

specimens had been collected by the Brazilian inverte-

brate zoologist Diva Diniz Corréa (1918-1993) while she

was on a Guggenheim Fellowship at the Pacific Marine

Station in Dillon Beach and SIO. Joel W. Hedgpeth

(honored with Elysia hedgpethi Marcus, 1961) helped her

collect. She had received her doctorate in 1948, under the

direction of Ernst Marcus. Upon his retirement, she was

appointed to his Chair, eventually serving as the first

female director of the Department of Zoology at the

Universidade de S4o Paulo.

Ernst and Eveline Marcus had both been born in Berlin

(in 1893 and 1901, respectively). He actually served in

World War I as a German soldier. After receiving his

doctorate in 1919, he was a museum curator of bryozoans

and then university professor. He married Eveline Du

Bois-Reymond in 1924, and they began their remarkable

scientific collaborations spanning decades and continents.

Anti-Jewish sentiment dismissed him from his profes-

sorship, and in 1936 they fled Nazi Germany to Brazil,

where he was appointed a professor of zoology at the

Universidade de Sao Paulo. Their earliest investigations in

their newly-adopted country were on “lesser known” in-

vertebrates such as bryozoans, nemerteans, and _tardi-

grades. He was honored with Brazilian citizenship in 1940.

However, during the height of World War IT, because of

his German ancestry, he was not allowed to study nor visit

the coast, so he concentrated on freshwater invertebrates.

Ernst and Eveline began studying opisthobranchs in the

early 1950s. After his death in 1968, Eveline Marcus

continued publishing, producing some 30 works on her

beloved opisthobranchs. She even visited the San Diego

area, meeting and collecting with various local re-

searchers, before her death in 1990.

Pioneering work by Wesley M. Farmer and Clinton L.

Collier in the early 1960s investigated the waters of

northwestern Mexico. They named four still-valid species

from the Gulf of California and Islas Cedros (Farmer,

1963; Collier and Farmer, 1964) and reported on the

distributions of opisthobranchs along the Pacific coast of

Baja California (Farmer and Collier, 1963). These were

the first nudibranch species named from specimens col-

lected in Mexico’s Sea of Cortez. Note that Lance’s (1962)

Histiomena convolvula has been synonymized with His-

tiomena marginata Orsted in Mérch, 1859.

Shortly afterward, Marcus and Marcus (1967) pub-

lished the first comprehensive report of opisthobranchs

Page 82

from the Gulf of California, noting that its nudibranch

fauna was not well known. They examined a collection of

animals sent by Peter E. Pickens, from the University of

Arizona’s field station at Puerto Pefiasco, Sonora. Sev-

enteen of the 20 new species they proposed are still

recognized today.

Returning to studies of heterobranchs in central Cal-

ifornia waters, MacFarland’s (1966) posthumously pub-

lished monograph introduced over a dozen new species.

Along with the Marcuses (1961 and 1967) publications, it

stands among the three pivotal works that “jump-started”

moder nudibranch research in the eastern Pacific. In

1969 and 1970, Richard A. Roller published several tax-

onomic updates to MacFarland’s monograph. Roller

(1930-1998) had taught high school biology in San Luis

Obispo for years before moving back east to indulge his

interest in antique fruit and canning jars. Early in 1969, he

and Steven J. Long co-founded the Opisthobranch

Newsletter, a monthly mailing of news, notes, references,

and queries and comments by various investigators. In

various iterations, this useful pre-Facebook communica-

tion traveled to the worldwide opisthobranch researchers

under the face of a postage stamp.

Checklists of records of nudibranch species from Santa

Barbara (Sphon and Lance, 1968) and San Luis Obispo

Counties (Roller and Long, 1969) gave a better under-

standing of the distributional patterns for nudibranchs

along the California coast. Gale G. Sphon (1934-1995)

worked as a curatorial assistant in the Santa Barbara

Museum of Natural History and the Los Angeles County

Natural History Museum. (On a very personal note, Gale

was responsible for introducing this author to nudibranchs

and their intertidal brilliance.) Working alongside these

Californian investigators, Gary McDonald, Dave Behrens,

Terry Gosliner, and others began what would be lifelong

(and still ongoing) studies on the taxonomy and natural

history of Heterobranchia.

While visiting Friday Harbor Laboratory, the English

investigator Anne Hurst (1967) described the egg masses

and veliger larvae of 30 species of opisthobranchs from the

San Juan Islands, Washington. She illustrated and defined

the patterns of their developmental shapes.

Research in the Gulf of California yielded additional

new species from that region (e.g., Farmer, 1978). With a

type locality in the southern Gulf, Chromodoris baumannni

(now in the genus Felimida) was the first species of nu-

dibranch ever named using scanning electron microscopy

to illustrate the radula (Bertsch, 1970). The first 3-D images

of the teeth were published as stereo SEMs in the de-

scription of another Gulf species (Bertsch et al., 1973). Line

drawings from light microscopes were replaced with this

new technology, which has become the standard for il-

lustrating the teeth and jaws of heterobranchs.

In situ field studies started to give a better under-

standing of nudibranch ecology. Gordon Robilliard (1971)

used scuba diving to document subtidal ecology in Puget

Sound. James W. Nybakken (1936-2009), professor of

biological sciences at the Moss Landing Marine Labo-

ratory, studied the intertidal community at Asilomar State

THE NAUTILUS, Vol. 134, No. 2

Beach (Monterey Peninsula). His studies (Nybakken,

1974, 1978) were the first quantitative studies of nudi-

branch assemblages on the Pacific coast. Over a 40-month

period, he used a timed-search methodology to calculate

seasonal and yearly variations of slug densities. These

results have been used to contrast findings at other eastern

and central Pacific sites (see Bertsch, 2011). For most

nudibranchs, using a timed search gives a better ac-

counting of their occurrence and density than does the

traditional transect/quadrant method. At Cape Arago,

Oregon, Jeffrey H. R. Goddard (1984) examined the

ecology and natural history of 46 species of opistho-

branchs, including descriptions of the egg masses and

larval development for 21 of those species.

Numerous experimental works were published on the

neurophysiology and behavior of Hermissenda (e.g.,

Alkon, 1980), Tritonia (e.g., Lohmann et al., 1991), and

Aplysia. Eric R. Kandel won the 2000 Nobel Prize in

Physiology of Medicine for his research on “signal

transduction in the nervous system” (Kandel, 2006). He

proposed the basis for memory in complex systems such as

the human brain by studying synaptic changes involved in

learning and memory in Aplysia californica, a far simpler

system. He isolated neuronal connections (before and

after conditioning) in the ganglia of A. californica. When

he was a youngster of 9 years old, he and his family had

fled the anti-Semite Nazi persecution in Vienna, settling in

New York. After training in medicine and a residency in

psychiatry, he began his research into the mechanistic

basis of learning. Multiple other species have been used in

pharmacological studies, looking for anti-viral, anti-

bacterial and anti-cancer chemicals (e.g., Turner et al.,

1998).

This period also marked a new high in the naming of

new species from the eastern Pacific, averaging almost

three per year. Papers by David W. Behrens and Terrence

M. Gosliner resulted in the description of some two dozen

new species and several new aeolid genera such as the

pretty Hermosita, and the Baja California-based Bajaeolis

(Gosliner and Behrens, 1986). Among other new species

were two highly appropriate patronyms: Eubranchus

steinbecki and Catriona (now Tenellia) rickettsi. Con-

tinuing the international nature of eastern Pacific marine

heterobranch research, Antonio Mozqueira Osuna was

the first Mexican citizen to name a species of nudibranch,

Tritonia myrakeenae. A student at Ciencias Marinas,

Universidad Aut6noma de Baja California, he had col-

lected several paratypes from E] Sauzal (several kilome-

ters north of Ensenada), while researching his Tesis de

Licenciatura.

7. 2001—Present: DNA, and Taxonomic and Spatial-

Temporal Changes

A. UNDERSTANDING TAXONOMY FROM A PAN-OCEANIC

PERSPECTIVE

The Swedish botanist C. Linnaeus classified living beings

in a hierarchical scheme and introduced binomial

H. Bertsch, 2020

nomenclature, simplifying the human desire to name.

Dating from his 1758 edition of Systema Naturae, this

system is still in use. In the next century, the basis for

classification changed from just shared morphological

similarities to evolutionary relationships. Lamarck’s 1809

Page 83

and Darwin’s 1868 drawings are the first know phyloge-

netic trees (Wheelis, 2007). Rudolph Bergh (1890)

published the first phylogeny of nudibranchs (Figure 12).

As global nudibranch research intensified during the

got century, numerous classifications were proposed by

Tritoniadae a

= Phyliroidae

Dendronotidae, Bornellae, ScyHaecne

”

Dotonidae, Lomanotidae

Pleuroleuridae

Tethymelibidae

Pulmonata

{(Pulmonata stylommatophora)

Branchiopneusta

(Puimonata basommatophora)

Pleurophyllidiadae

‘

; 2

: :

| i

a" 4

(Janidae) =

Aeolidiadae

{Phy llobranchidae)

Ascoglossa

Steganobranchia

(Tectibranchia)

Figure 12. First phylogenetic tree of nudibranchs. (Bergh, 1890: 7)

Page 84

European researchers to explain the evolutionary rela-

tionships within this group, e.g., the Belgian Pelseneer

(1894), the Swedish Odhner (1934), and the German

Boettger (1955). In a comprehensive study of opistho-

branch phylogeny, Ghiselin (1966) used a functional

analysis of the reproductive system “to take causes of

evolutionary change into account in reconstructing the

sequences of modification.”

In the 1980s, phylogenetic studies of Opisthobranchia

were revolutionized by the use of Hennigian calculable

phylogenies. Hennig (1966) had proposed analyzing

shared and derived characters to determine the evolu-

tionary relationships among taxa at various hierarchical

levels. Cladistic analyses based on morpho-anatomical

characters were used to describe relations between ma-

jor subgroups, families and genera (see Wagele et al.,

2014, for an exhaustive list). Especially noteworthy was

Gerhard Haszprunar (1985) formally establishing Het-

erobranchia as a phylogenetic clade. A major taxonomic

upheaval occurred as phylogenetic studies gained a new

tool, the genetic analysis of RNA and DNA sequences.

The first genetic analyses of phylogeny (e.g., Tillier

et al., 1994; Thollesson, 1999a, b) used only a few mi-

tochondrial RNA genes, based on a small sampling of

species. Soon additional genes were studied, from a

greater breadth of species. The monophyly of Euthyneura

and Opisthobranchia were debated (e.g., Grande et al.,

2004a, b; Vonnemann et al. 2005; Dinapoli and

Klussmann-Kolb, 2009) and different groups were in-

cluded or excluded from traditional clades.

Multiple studies showed the use of the clade Opistho-

branchia in the traditional sense was no longer acceptable

(Thollesson, 1999b; Schrédl et al., 2011). Sacoglossa was

separated from the traditional orders of Opisthobranchia

and placed as an early divergence within the Pan-pulmonate

lineage. Nudibranchs are no longer the “crown” of the

Cephalaspidea-Anaspidea-Notaspidean lineage. Gone is the

tri-partite division of Gastropoda into Prosobranchia,

Opisthobranchia, and Pulmonata; gone are the Opistho-

branchia with their five major orders. Who’s related to

whom is no longer what had been thought (Wagele et al.,

2014; Kano et al., 2016).

B. EASTERN PACIFIC STUDIES AND INTERNATIONAL

COOPERATION

Eastern Pacific sea slugs were quickly caught up in this

new gene-based taxonomic volatility. Four California

museum or university laboratories were dedicated to

heterobranch research: MacFarland’s modern California

Academy of Sciences (under Terrence M. Gosliner),

Natural History Museum of Los Angeles County (Angel

Valdés, currently Jann Vendetti), California State Uni-

versity at Los Angeles (Patrick J. Krug), and California

State Polytechnic University at Pomona (A. Valdés). In-

dependently or collaboratively, researchers from Europe

also studied eastern Pacific nudibranchs and their allies,

including Alexander Martynov and Tatiana Korshunova

(Moscow State University, Russia) and J. Lucas Cervera

THE NAUTILUS, Vol. 134, No. 2

(Universidad de Cadiz, Spain). These investigators and

their students have studied families, genera, and species

occurring in multiple circumglobal marine provinces,

including those in the eastern Pacific. Over 60 species of

Heterobranchia have been named from the eastern Pa-

cific during this historical period. Species thought to have

occurred in multiple provinces have been named as new,

with restricted distributional patterns of the different

populations. Eastern Pacific specimens originally identi-

fied as the Mediterranean Limenandra nodosa Haefel-

finger and Stamm, 1958, are now Limenandra confusa,

and the Caribbean Polybranchia viridis (Deshayes, 1857)

from our coastline is now Polybranchia mexicana. Even

along the North American Pacific coastline, cryptic and

pseudo-cryptic species have been discovered with dif-

fering northern and southern distributional patterns. For

some (e.g., Diaulula odonoghuei and Hermissenda opa-

lescens) prior synonyms have been restored; for others,

new species names have been proposed (e.g., Limacia

mcdonaldi and Doriopsilla davebehrensi). There have

been scores of taxonomic changes since the publication of

Eastern Pacific Nudibranchs (Behrens and Hermosillo,

2005), which have necessitated a new, fully revised and

updated edition. Admittedly, individually mentioning

~ each and every one of these contributions would be ex-

cessive. Hence, only a few representative papers and

authors have been highlighted here.

Research in the subtropical and tropical waters of the

eastern Pacific now includes the field work of Mexican and

Costa Rican workers studying their nations’ fauna. After

completing graduate student theses, Alicia Hermosillo

McGowan (studying the heterobranchs of Bahia de Ban-

deras, Jalisco-Nayarit, Mexico), Orso Angulo Campillo (at

La Paz, Baja California Sur, Mexico), and Yolanda Cama-

cho-Garcfa (Costa Rica) have gone on to name several

dozen nudibranch species from these waters (e.g., Polycera

kaiserae, Marionia kinoi, and Jorunna osae). The active

work of these and other Latin American investigators have

greatly enhanced international research efforts across ma-

rine faunal provinces and nations in the eastern Pacific.

Long-term subtidal natural history studies using

Nybakken’s (1978) timed-search method (Hermosillo,

2006, three years; Bertsch, 2019, 30+ years), have yielded

information on annual and seasonal variations, feeding,

reproduction, and bathymetry of heterobranch species

communities in the Gulf of California and along the

southwestern Mexican coastline.

Using data from Jim Lance’s La Jolla surveys and more

recent observations throughout southern California, the

extinction and recovery of the brilliant blue and gold

nudibranch Felimare californiensis has been documented

(Goddard et al., 2013; Hoover et al., 2017).

For years, species common in the Gulf of California

have been sporadically reported from southern California.

Species such as Pleurobranchus digueti, Berthellina ilisima,

and Flabellina bertschi have been cited as “El Nifio oc-

currences,” but without confirmatory timed data sets

available. Recent work by a cadre of researchers in the

Californian and Oregonian faunal provinces has correlated

H. Bertsch, 2020

northward range shifts of heterobranch species with dis-

tinct periods of El Nifio phenomena (Goddard et al., 2016,

and 2018). With the anthropogenic-caused climatic

changes endangering both terrestrial and marine habitats,

these studies are important to determine adaptability and

survivability of these organisms with range changes under

climatic stress, and to formulate positive actions that can be

taken by humans to ensure marine biodiversity conserva-

tion (Tittensor et al., 2019).

Our knowledge of eastern Pacific heterobranchs is

growing and still being written. Conserving these organisms

and their habitats is an essential part of that effort.

Mi.

“If facts are the seeds that later produce knowledge and

wisdom, then the emotions and the impressions of the senses

are the fertile soil in which the seeds must grow. The years of

early childhood are the time to prepare the soil. Once the

emotions have been aroused—a sense of the beautiful, the

excitement of the new and the unknown, a feeling of

sympathy, pity, admiration or love—then we wish for

knowledge about the subject of our emotional response.

Once found, it has lasting meaning.”

Rachel Carson, 1965

The Sense of Wonder

The study of biology is historical (Mayr, 2004). It is a record

of the evolutionary changes wrought by natural selection on

the genotypic and phenotypic variations of living beings.

The unique global ecosystem is a nexus of biological,

chemical, and geological interactions, forming that synergy

called life. Steinbeck and Ricketts (1941) argued against

teleology when they wrote there is no why, that life just is.

But because it is, it deserves to be.

Observation, hypothesis, experimentation and theory

become science only with communication. The ethics of

science demands truth in our research and in our

communication. Predictability of the results ranges from

the effects of mass and distance on gravity to the future

of life in the Anthropocene. Predicting history can only

be based on history. What will happen if human-caused

global climate change, that has resulted in unwanted

adverse changes and extinctions, continues? As in evo-

lution, what is done today will create the future. Care for

tomorrow is scientific. Conservation of earth’s ecosys-

tems and their biodiversity is science communicated

well. Doing science is truly for the children and the

future generations of all life. Whatever that future be-

comes depends on our research and actions today. The

history will be written by the children.

ACKNOWLEDGMENTS

I am grateful to Robert Dees (Cambria, California) and

Juan Lucas Cervera (Cadiz, Spain) for their generous and

invaluable assistance with the writing of this manuscript,

and to Jan Kocian (Whidbey Island, Washington) for

allowing me to use his marvelous drawing.

Page 85

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Research Note

Page 89

First ex-situ observation of Vasula deltoidea

(Lamarck, 1822) (Gastropoda: Muricidae)

mating and egg-laying with emphasis on the

potential for hatchery-reared individuals to

aid coral reef restoration

Gabriel A. Delgado

Einat Sandbank

William C. Sharp

Florida Fish and Wildlife Conservation Commission

Fish and Wildlife Research Institute

Marathon, FL 33050, USA

Gabriel. [email protected]

There is a long history of raising gastropods under

hatchery conditions for stock enhancement and food

production, but another application of gastropod aqua-

culture could be to aid coral reef ecosystem management

and restoration (i.e., conservation aquaculture). Florida’s

coral reefs currently exist in a degraded state (Jackson

et al., 2014), which has given rise to restoration efforts

predominantly using outplanted staghorn coral, Acropora

cervicornis (Lamarck, 1816) (Young et al., 2012; National

Oceanic and Atmospheric Administration, 2020). However,

the corallivorous gastropod Coralliophila galea (Dillwyn,

1823) is a major predator on acroporids (Potkamp et al.,

2017a, b). Corallivory is a natural predator-prey interac-

tion, but, in degraded coral reef ecosystems, corallivores

can be a substantial impediment to recovery by creating

synergies with other stressors thus augmenting coral mor-

tality (Rice et al., 2019). To counteract this, the use of native,

predatory gastropods to control corallivorous species has

been espoused. For example, it has been suggested to have a

ready supply of hatchery-reared Giant Triton snails,

Charonia tritonis (Linnaeus, 1758), to deal with sudden

outbreaks of Crown-of-thorns Starfish (Acanthaster planci

species complex) on the Great Barrier Reef (Hall et al.,

2017). In Florida, laboratory and field studies have dem-

onstrated that the presence of the Deltoid Rock Snail,

Vasula deltoidea (Lamarck, 1822), reduced the effects of

predation by C. galea on A. cervicornis through direct

consumption and also by provoking an escape response in C.

galea (Delgado and Sharp, 2020).

To further these conservation aquaculture efforts, we

describe herein the first ex-situ observation of V. deltoidea

mating, egg laying, and early veliger growth. Vasula deltoidea

individuals were collected from the Florida Keys reef tract

and held for an acclimation period of at least one week under

ambient nearshore seawater conditions. A temperature-

controlled, 379-liter aquarium array (Marineland®) with

centralized mechanical, biological, and chemical filtration

was used for the trials. The array consisted of three separate

114-liter aquariums, each divided into three equal sections

by perforated acrylic partitions, yielding a total of nine

physically isolated sections all of which were subjected to the

same recirculating water mass. Due to the difficulty in sexing

individuals, each of the nine sections housed a pair of

unsexed V. deltoidea that were monitored for up to 30 days.

Vasula deltoidea were fed live C. galea and/or Lithopoma

americanum (Gmelin, 1791). Trials were conducted at two

temperatures, 23°C and 30C, which typify winter and

summer water temperatures along the Florida Keys reef

tract, so that a total of 18 pairs were observed. The shell

Figures 1-2. Vasula deltoidea female in the process of laying the first of her egg clusters behind one of the slits in the acrylic partition

in our aquarium array. The female and the egg cluster are both below the water line. 1. Ventral view. 2. Dorsal view.

Page 90

lengths of these individuals ranged from 29.0-37.8 mm; the

mean (+ one SE) was 32.9 + 0.31 mm. Synthetic seawater

(Instant Ocean® Reef Crystals) at 35 ppt was used. The

aquarium array had a flow rate of 4,540 liters per hour;

lighting was on a 12-hour light-dark cycle and consisted of T5

10,000K and actinic fluorescent bulbs.

During the first ten days of one of the summer trials, we

observed one pair of V. deltoidea copulating. The shell

lengths of these two individuals were 32.7 and 34.8 mm.

The female laid two clusters of egg capsules in four days

(Figures 1-4). Each cluster took approximately 24 hours

to complete. The first cluster contained 74 individual egg

capsules, whereas the second had 41 (Figures 3-4). The

capsules were round and flattened (Figures 3-4) and

contained dark brown veligers (Figure 5). The number of

developing veligers in five haphazardly chosen egg cap-

sules was counted using a stereomicroscope. The mean

number of veligers per capsule was 149.6 + 4.28. Using

this calculation and the number of capsules in each egg

cluster, we estimated that the first cluster contained

11,070 + 317 veligers; the second cluster had 6,134 +

Figures 3-4. Post-hatch photographs of the two egg clusters

laid by the Vasula deltoidea female. 3. The first egg cluster

contained 74 individual, adjacent egg capsules. 4. The second

egg cluster, laid 2 days later, had 41 egg capsules.

THE NAUTILUS, Vol. 134, No. 2

Figure 5. Photograph of the developing Vasula deltoidea

veligers within one of the egg capsules; the veligers are 14 days

old.

176. The water temperature in which the V. deltoidea and

the developing veligers were held was 29.4 + 0.05 C.

The eggs hatched after an incubation period of 21 days.

The veligers from the first cluster were raised in a 21-liter

aquarium. This equates to a stocking density of 530 ve-

ligers per liter. The veligers were fed approximately 4 ml

of AlgaGen PhycoPure™ (a live mix of microalgal species)

per day. To track growth, we measured the larval shell

length of five haphazardly chosen veligers on days 1, 2, 3,

6, and 10. Newly hatched veligers were approximately 300

wm and grew slowly, reaching approximately 340 pm on

375

350

325 | :

300 +

shell length (microns)

275 +

days post-hatch

Figure 6. The mean shell length of the post-hatch Vasula

deltoidea veligers over time. Error bars represent + one stan-

dard error.

G.A. Delgado et al., 2020

day 10 (Figure 6), after which all the veligers unexpectedly

died. Water temperature was 29.8 + 0.03°C; salinity was

35 ppt.

Our findings are consistent with the only other study

(Lewis, 1960), as far as we know, that describes the re-

productive aspects of Vasula deltoidea (Lewis, 1960).

That study, conducted in Barbados, reported that V.

deltoidea laid egg clusters when water temperatures were

approximately 28°C, quite similar to our simulated

summer temperatures. Lewis (1960) also observed that V.

deltoidea \aid egg clusters in holes and depressions below

the water’s surface. Our aquarium array consisted of

smooth surfaces except for the perforations in the acrylic

partitions, which provided V. deltoidea individuals a

substitute for natural topography (Figures 1-2). We note

that two other females laid egg clusters on the Vexar®

mesh that covered the drainpipe in our acclimation tank,

but no quantitative data were recorded in these instances.

Evidently, the broodstock environment must have a

measure of topographic complexity with holes or cavities

in which females can lay their egg clusters. Nonetheless,

further studies on broodstock maintenance are warranted.

For example, broodstock conditioning can probably be

improved through diet refinement as V. deltoidea will

consume other mollusks besides Coralliophila galea and

Lithopoma americanum (Delgado and Sharp, 2020). In

addition, the frequency of copulation can probably be

increased by sexing individuals or perhaps by keeping a

group of more than two as V. deltoidea may prefer to mate

en masse as in the confamilial Thaisella chocolata (Duclos,

1832) (Romero et al., 2004).

The physical characteristics that we detail for the V.

deltoidea egg capsules and veligers are corroborated by

Lewis (1960), but that study did not document devel-

opment time or fecundity. The intracapsular development

time of 21 days that we observed is comparable to other

species within the subfamily (Romero et al., 2004).

Stramonita rustica (Lamarck, 1822), a confamilial species

also present in Florida, was found to have a similar

number of veligers per spawn as our results; however,

unlike V. deltoidea’s flat and round egg capsules, S.

rustica’s egg capsules are vasiform in shape (D’Asaro,

1970). Lewis (1960) reported larger V. deltoidea veligers

at hatch (360 wm) compared to those that we observed

(300 ym), but the veligers in both studies survived only a

few days post-hatch. Research into optimal water quality

parameters, veliger stocking densities, and veliger nutri-

tional requirements can probably improve survival.

However, if V. deltoidea has a protracted (e.g., 3-

4 months) larval phase like other members of its family

(D’Asaro, 1970; Romero et al., 2004), raising the veligers

to settlement may not be practicable even with im-

provements to larviculture techniques.

At present, most coral reef restoration efforts have been

experimental or limited in spatial scale (National Acad-

emies of Sciences, Engineering, and Medicine, 2019).

However, the Florida Keys National Marine Sanctuary is

undertaking a massive project to restore seven reefs using

almost 500,000 coral colonies, 40% of which will be

Page 91

acroporids (National Oceanic and Atmospheric Admin-

istration, 2020). Incorporating hatchery-reared V. del-

toidea into reef restoration may increase the survival of the

outplanted acroporids by mitigating C. galea corallivory

(Delgado and Sharp, 2020). Our ex-situ observations of V.

deltoidea mating and egg laying show some promise in this

regard; however, further broodstock and _ larviculture

studies are needed to determine if cultivating V. deltoidea

for conservation purposes is feasible. If so, V. deltoidea

may prove a valuable addition to coral reef ecosystem

restoration efforts.

LITERATURE CITED

D’Asaro, C.N. 1970. Egg capsules of prosobranch mollusks from

South Florida and The Bahamas and notes on spawning in

the laboratory. Bulletin of Marine Science 20: 414440.

Delgado, G.A. and W.C. Sharp. 2020. Capitalizing on an eco-

logical process to aid coral reef ecosystem restoration: Can

gastropod trophodynamics enhance coral survival? Coral

Reefs 39: 319-330.

Hall, M.R., C.A. Motti, and F. Kroon. 2017. The Potential Role

of the Giant Triton Snail, Charonia tritonis (Gastropoda:

Ranellidae) in Mitigating Population Outbreaks of the

Crown-of-Thorns Starfish. Integrated Pest Management of

Crown-of-Thorns Starfish. Report to the National Envi-

ronmental Science Programme. Reef and Rainforest Re-

search Centre Limited, Cairns, 58 pp.

Jackson, J.B.C., M.K. Donovan, K.L. Cramer, and V.V. Lam.

2014. Status and Trends of Caribbean Coral Reefs:

1970-2012. Global Coral Reef Monitoring Network,

IUCN, Gland, Switzerland. 304 pp.

Lewis, J.B. 1960. The fauna of rocky shores of Barbados, West

Indies. Canadian Journal of Zoology 38: 391-435.

National Academies of Sciences, Engineering, and Medicine.

2019. A Research Review of Interventions to Increase the

Persistence and Resilience of Coral Reefs. The National

Academies Press, Washington, DC, 258 pp.

National Oceanic and Atmospheric Administration. 2020. Re-

storing Seven Iconic Reefs: A Mission to Recover the Coral

Reefs of the Florida Keys. National Oceanic and Atmo-

spheric Administration, Washington, DC, 45 pp.

Potkamp, G., M.J.A. Vermeij, and B.W. Hoeksema. 2017a.

Host-dependent variation in density of corallivorous snails

(Coralliophila spp.) at Curacao, southern Caribbean. Ma-

rine Biodiversity 47: 91-99.

Potkamp, G., M.J.A. Vermeij, and B.W. Hoeksema. 2017b. Genetic

and morphological variation in corallivorous snails (Cor-

alliophila spp.) livmg on different host corals at Curagao,

southern Caribbean. Contributions to Zoology 86: 111-144.

Rice, M.M., L. Ezzat, and D.E. Burkepile. 2019. Corallivory in the

Anthropocene: Interactive effects of anthropogenic stressors

and corallivory on coral reefs. Frontiers in Marine Science 5:

525.

Romero, M.S., C.S. Gallardo, and G. Bellolio. 2004. Egg laying

and embryonic-larval development in the snail Thais

(Stramonita) chocolata (Duclos, 1832) with observations on

its evolutionary relationships within the Muricidae. Marine

Biology 145: 681-692.

Young, C.N., S.A. Schopmeyer, and D. Lirman. 2012. A review

of reef restoration and coral propagation using the

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Atlantic. Bulletin of Marine Science 88: 1075-1098.

THE NAUTILUS 134(2):92-94, 2020

Research Note

Page 92

Range and dietary expansion of the

nudibranch Felimare ruthae (Ev. Marcus

and Hughes, 1972) (Gastropoda:

Chromodorididae)

Michael L. Middlebrooks

Daniela Gutierrez-Andrade

Sarah E. Cuccinello

Department.of Biology

University of Tampa

Tampa, FL 33606, USA

[email protected]

Many nudibranch sea slugs have very specific diets; in

particular, the family Chromodorididae Bergh, 1891 are

oligophagous sponge feeders (Rudman and Bergquist,

2007). Many chromodorids only consume one species of

sponge (Rudman and Bergquist, 2007) and rely on the

sponge not only as food, but also for defensive secondary

metabolites (Faulkner and Ghiselin, 1983; Cinimo and

Ghiselin, 1999). The diet of many chromodorids, how-

ever, is poorly understood due to their rarity, poor doc-

umentation, and difficulty in identifying their sponge food

(Rudman and Bergquist, 2007).

Recent studies, and the increase in popularity of nu-

dibranch underwater photography and public records,

have improved our knowledge of the geographic ranges of

many species of nudibranchs. However, range boundaries

are often not well established, and the distribution of

certain species remains obscure. Recently, several nudi-

branch species, including chromodorids, have undergone

range expansions (Ozcan et al., 2010; Padula et al., 2011;

Nimbs et al., 2016). Although some geographic shifts have

occurred due to natural reasons (Borg et al., 2009), ac-

cidental introductions (Ozcan et al., 2010; Lipej and

Mavric, 2017) and climate change (Goddard et al., 2011;

Nimbs et al., 2016) might have also contributed to the

geographic spread of sea slugs.

Felimare ruthae (Ev. Marcus and Hughes, 1974)

(Figure 1) is a small chromodorid ranging in size from 9 to

38 mm (Meyer, 1977; Humann, 1992). It is dark blue with

5 to 6 parallel lines that extend along the dorsum and a

thick white marginal band with a bright yellow border (Ev.

Marcus and Hughes, 1974; Ortea et al., 1996). The nu-

dibranch is typically found at depths between 1-20 m in

areas with moderate currents (Humann, 1992; Ortigosa

and Simoes, 2019). It occurs throughout the Caribbean, as

far south as Venezuela and north as the Bahamas (Valdes

et al., 2006). Additionally, it can also be found in the

southern Gulf of Mexico, inhabiting coastal reefs of the

Yucatan Peninsula (Ortigosa et al., 2013; 2015; Ortigosa

and Sim6des, 2019). Felimare ruthae has been reported

to feed on sponges Dysidea janiae Duchassaing and

Michelotti, 1864 (Humann, 1992; Valdés et al., 2006) and

D. etheria Laubenfels, 1936 (Rudman and Bergquist,

2007).

In June 2019, we were informed by local divers that

Felimare ruthae had appeared in large numbers on

limestone ledges located offshore of Clearwater, Florida,

from where it had never been reported. These ledges

are ~24 km offshore, rising 1-2 m off the seafloor in

~12-15 m depth, and supporting a diverse benthic

community. On June 5, 2019, the area known as the Miss

D Ledge (28°04.145° N, 83°00.392° W) was visited via

SCUBA. Felimare ruthae was primarily found on medium

to large demosponges. Up to five individuals were on a

single sponge and several of them were observed feeding

upon the sponges. On June 21, 2019, we conducted

formal surveys of the sponges on that site. In total, 35

sponges were surveyed of which 12 harbored a total of 16

F. ruthae. Sponges were an average diameter of 56cm +

13 cm. One slug was crawling on the limestone substrate.

Tissue samples of several sponges were taken for iden-

tification. One other nudibranch, F. picta Philippi, 1836,

also frequently occurs in this habitat feeding on species of

Dysidea Johnston, 1842.

Morphological examination of the sponge tissue was

conducted using the descriptions in Hooper and van Soest

(2002). The sponge was lacking laminar structure, spic-

ules, and fine collagenous fibers. The fibers present were

homogenous suggesting it belongs in the family Spon-

giidae Gray, 1867. The sponge also had an unarmored

surface, simple primary fibers without fascicles, and was

not lacunose, suggesting it belongs in the genus Spongia

Linnaeus, 1759.

DNA was extracted from an alcohol-preserved sample

of sponge tissue using the DNeasy Blood and Tissue Kit

(Qiagen). We used degenerate PCR primers to amplify

the 28S rDNA C-Region (F: 5’-GAAAAGAACTTT-

CRARAGAGAG [3 Ri - TCECGTGLELCAAGAGGG-

G-3’) (Chombard et. al, 1998). A three-step PCR am-

plification program included initial denaturing at 94°C

for 3 minutes, followed by 35 cycles of 94°C for 30

seconds, 45°C for seconds, and 72°C for 1 minute, and a

final extension at 72°C for 5 minutes. Sanger-sequencing

(Genewiz) was performed using purified PCR product.

Sequence results were queried using the BLAST alignment

tool. Results of the BLAST search showed that the lowest

E-value of 5e-36 correlated with Spongia sp. (Genbank

accession number KC869488. 1).

Although chromodorids typically have very narrow

diets, a few species have been documented consuming a

wider variety of foods. For example, species in the genus

Ceratosoma Adams and Reeve, 1850 exclusively eat

dysideid sponges; however, C. amoenum Cheeseman,

1886 is also found feeding on species of the thorectid

sponge Semitaspongia Cook and Bergquist, 2000 (Rudman

M.L. Middlebrooks et al., 2020

i ee

Figure 1. Felimare ruthae on Spongia species, at Miss D

Ledge, off Clearwater, Florida. :

and Bergquist, 2007). Species in the genus Felimare Ev.

Marcus and Er. Marcus, 1967 seem to have evolved

feeding on dysideid sponges (Johnson and Gosliner 2012);

however, one Mediterranean species, F. tricolor Cantraine,

1835, sometimes consumes Spongia species (Furfaro et al.,

2016). Either some chromodorid species can opportunis-

tically feed on other sponges or specific populations have

successfully changed diet.

Switching between diets, however, is not a trivial

matter. The chemical metabolites produced by sponges

can vary widely (Thoms and Schupp, 2007). For example,

species in the family Dsyideidae produce sesquiter-

penes, while those in the Spongiidae produce ses-

terterpenes (Rudman and Bergquist, 2007). By changing

diets between these sponge families, F. ruthae not only

has to adapt to metabolize a different suite of chemicals,

but may also need to modify these metabolites for its own

defense.

It is unclear what caused this range expansion, but the

shift in diet may have contributed. It will be worthwhile to

determine whether populations of F. ruthae from other

areas also feed on Spongia species or if this is limited to

Florida populations. It is unclear if this range expansion

will be permanent; however, diver reports from early 2020

continue to indicate local occurrences of F. ruthae. Range

expansions by other nudibranchs have been shown to

modify community structure (Allmon et al., 1988), sug-

gesting that continued monitoring would be worthwhile.

ACKNOWLEDGMENTS

We wish to thank Ryan Nelson, Seth Pikal, and Tanks-A-

Lot Dive Charters for alerting us about the slug and

assisting with surveys. We thank Tom Dix at Hillsborough

County EPC for morphological identification of the

sponge. The research was funded, in part, by a University

of Tampa Summer Undergraduate Research Fellowship

awarded to DGA.

Page 93

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