Phanerophthalmus luteus, (Quoy and Gaimard, 1833) (Quoy and Gaimard, 1833)

Ghiselin, Michael T. & Lipps, Jere H., 2019, The Sea Slug Phanerophthalmus luteus (Gastropoda: Opisthobranchia) and its Habitat and Ecology at the Marine Jellyfish Lake (Ongeim’l Tketau), Palau, Western Pacific Ocean, Proceedings of the California Academy of Sciences 65 (8), pp. 181-194 : 189-191

Morphology and Systematics of P. luteus

The animals of interest are sea slugs of the order Cephalaspidea , assigned by us to Phanerophthalmus luteus (Quoy and Gaimard, 1833) . Originally, we assigned our specimens to P. smaragdinus (Ruppell and Leuckart 1831) , as did others ( Patris et al. 2012), but in a recent revision of species of Phanerophthalmus, Austin, Gosliner, and Malaquias (2018) did not recognize P. smaragdinus , putting it in synonymy with several other species. Using their criteria, our specimens are most similar to P. luteus . We base this determination on the facts that the animals are generally green, greenish white or greenish blue, the shell is partly exposed by the mantle cavity, and P. luteus ’s known distribution embraces Palau. The other species that biogeographically overlap in the western Pacific are distinctly different and not similar to P. luteus . Other morphologic and genetic details of this species are given in Rudman (1972) and Austin, Gosliner, and Malaquias (2018).

In Jellyfish Lake, the slugs were of unusually large size. The largest specimen in Jellyfish Lake was 55 mm long and 33 mm wide which is among the largest individual of any species in the genus. The slugs at Jellyfish Lake were clearly larger and more abundant than in open ocean situations elsewhere in the Indo-Pacific. This is a common feature of organisms found in these restrictive and isolated marine lakes. We also know of one well-documented case of opisthobranchs sometimes attaining unusually large size when they occur outside of their ordinary habitat, the anaspidean Phyllaplysia taylori Dall, 1900 ( Beeman 1970). In northern California and elsewhere in the Oregonian province, these P. taylori are common and well camouflaged on the sea-grass Zostera marina . They feed upon diatoms and other organisms that live on the plants. Animals kept in outdoor tanks at the Hopkins Marine Station flourished off of the sea-grass. They attained a much larger size than those from nearby Elkhorn slough (respectively a maximum weight of 15.03 g and 1.6 g). Why P. luteus should attain larger size in unusual habitats is unknown but may be related to food supply, as implicated by the Hopkins study, or by a reduction of predation on mid- or larger sized animals. Certainly, the habitats of P. luteus in Jellyfish Lake are richer in organic materials, algae, phytodetritus, and periphyton growing on the substrates along with the slugs. Like Mastigias papua etpisoni , P. luteus could also show genetic differences once they are analyzed from other occurrences of this species in the central and western Pacific Ocean.

Egg Masses

In Jellyfish Lake, P. luteus lays very abundant egg masses attached to algae ( Fig. 7 ) or other substrates at particular times during the year. The difference in daylight distribution of the egg masses and the animals themselves could mean that the animals move toward shallower water or stay hidden during the day. Our study, done in the middle of the day when the animals were found under algae, logs or the edges of rocks, indicates that the animals likely emerge from hiding at night when they then deposit the egg masses. The egg masses of P. luteus differed from those of P. perpallidus from Bali and P. purpura from Maui which were much smaller, 12 mm and 22 mm, had a somewhat different shape and color ( Austin, Gosliner, and Malaquias 2018, fig. 29). The egg masses of opisthobranchs, however, quite generally take up water with time, hence their size is not very informative. Further study of Phanerophthalmus eggs is warranted.

Biogeography

The genus Phanerophthalmus is distributed from the east coast of South Africa, Kenya, Reunion Island, and Madagascar, across the Indian Ocean to the Seychelles and Lakshadweep, Nicobar and Andaman Islands and through Papua New Guinea, New Caledonia, the Philippines, to Palau, Guam, Hawaii, and Japan ( Kay 1979; Colin and Arneson 1995; Gosliner, Behrens, and Valdés 2008; Apte 2009; Sreeraj, Sivaperuman, and Raghunathan 2012a, 2012b; Narayana and Mohanraju 2013; Kiruba-Sankar et al. 2016; Yonow and Jensen 2018; Austin, Gosliner, and Malaquias 2018). It likely occurs more widely in the Indo-Pacific but its species are rarely reported animals. The various species have different biogeographic ranges ( Austin, Gosliner, and Malaquias 2018).

The occurrence of P. luteus at Jellyfish Lake is well within the known biogeographic range of the species ( Fig. 8 ) in the central and western Pacific Ocean ( Austin, Gosliner, and Malaquias 2018, fig 23). The P. luteus in Jellyfish Lake are generally larger and more abundant than those found elsewhere in its biogeographic range. This is likely due to more abundant food, fewer predators, less seasonal change and quieter waters inside the lake. The reefs in the lagoon have, however, quite different habitats than those found within Jellyfish Lake. The reefs are in open ocean settings without large organic inputs, less benthic algae, variable temperatures, and generally rougher water while the mangrove-associated habitats in the lake had much organic matter and debris and lower oxygen content not found outside the enclosed lakes.

Habitat and Ecology

In general, P. luteus seems to occur in water shallower than 10 m across its biogeographic area including in rocky intertidal, coral rubble, back reef, organic-rich mangrove and algal habitats. That description fits well with the Jellyfish Lake occurrence where mangroves hang over the water and the sediments are rich in organic matter that falls into the lake ( Fig. 3 ). The foraminifera from the lake are a fauna that that is typically associated with mangroves elsewhere in the Pacific (Langer and Lipps 2003, 2006; Lipps and Langer 1999). Indeed, these mangrove faunas are consistent across most ocean basins and hence provide excellent markers for sea level and tidal changes (Horton et. al 2005).

Species of Phanerophthalmus were assumed to be herbivorous ( Rudman 1972) on algae, although only one species P. luteus of several examined had food in their guts ( Austin, Gosliner, and Malaquias 2018, fig. 28). That specimen had several species of centric and pennate diatoms in its gut. Diatoms, both benthic and the planktonic Chaetoceros affinis , occur in abundance in Jellyfish Lake ( Hamner, Gilmer, and Hamner 1982; Hara et al. 2002; Konno et al. 2010). P. luteus likely consumes both types of diatoms, the benthic ones as part of the periphyton on substrates where it lives and the planktonic kinds after they settled to the algae or sediment on the bottom. Periphyton is abundant on logs, smaller plant debris, on algae but less so on muddy substrata.

Jellyfish Lake, usually considered ecologically stable, has experienced changes in temperature, salinity and other factors due to El Niño events ( Dawson, Martin, and Penland 2001; Martin et al. 2006; Patris et al. 2012), and longer-term sea level and climate changes (Dickinson and Athens 2007). During the 1997–1999 El Niño, the Golden Jellyfish Mastigias papua etpisoni containing symbionts in their tissues declined to low numbers from a population in the millions and the Moon Jelly Aurelia was completely extirpated from the lake and did not recover ( Patris et al. 2012). On a longer time of ~ 100 years ago, a core taken at 10 m depth in Jellyfish Lake showed a change from older carbonate to the present siliceous sediment and also in the benthic foraminiferal biota during the “Little Ice Age” time ( Kawagata 2005). Over 1000s of years, sea level has risen first at 4000 years ago higher than present sea level but then retreating to the present level at least by 2000 years ago. These events indicate that the lake is a dynamic place over times longer than what ecologists have been able to study that likely impacted populations of animals, including P. luteus , plants and microbes.

Figures

FIGURE 7. Egg masses (more or less spherical to oblong white objects) of Phanerophthalmus luteus attached to filamentous and other algae on a slope in Jellyfish Lake. Photograph taken November 16, 2009, courtesy of Lori J. Bell.

FIGURE 8. Central and Western Pacific showing the distribution of Phanerophthalmus luteus (black stars) and the location of Jellyfish Lake, Palau (large gray star). Modified from distribution map for P. luteus in Austin, Gosliner, and Malaquias (2018, fig. 23).

FIGURE 3. Vegetation of Jellyfish Lake, Mecherchar Island. A. The lake, slightly less than 400 m long, is in a hole at least 230 m deep (150 to 200 m from the top of the hole to the Lake’s surface and 30 m to the bottom of the lake) in the Miocene limestone. North is at the top of the image. B. Dense terrestrial vegetation, including mangroves at the lake edges, hangs over the lake. The surrounding vegetation contributes organic debris to the lake. C. Bottom of the lake from 0 to 13 m is covered with plant debris and algal growth. Photograph is at 2 m deep looking down slope. D. One of many logs that have fallen into the lake and are now inhabited by a wide variety of algae and animals including P. luteus. View is down the log from a depth of about 0.5 m. Credits: A. Aerial photograph courtesy of Dr. Pat Colin. B.-D. Photographs by Jere H. Lipps, 2013.