This section continues with information on diets and feeding ecology of west-coast nudibranch & relatives genera N-P. Information on diets and feeding ecology of other west-coast genera can be found in other sections:
PREFERRED FOODS FEEDING ECOLOGY & GROWTH: GENERA A-C,
PREFERRED FOODS FEEDING ECOLOGY & GROWTH: GENERA H-M,
PREFERRED FOODS FEEDING ECOLOGY & GROWTH: GENERA R-T,
PREFERRED FOODS FEEDING ECOLOGY & GROWTH: SACOGLOSSANS, and INGESTIVE CONDITIONING.

Navanax

The large (to 12cm) cephalaspidean Navanax inermis (photo above Left) eats many types of opisthobranchs.  An early report of its feeding behaviour in San Diego, California indicates that it locates its prey by contact chemoreception of the mucus-impregnated trail of its prey. Apparently, it is incapable of distance chemoreception. 

To test this the author guides a crawling prey Bulla sp. (another cephalaspidean: photo below Left) in an aquarium in the laboratory in such as way that it leaves a mucous track in the shape of an open reverse-9 shape on the surface of the sand.  The Bulla is allowed to rest at the end of the track.  A Navanax is then placed at the start of the trail. It follows the trail faithfully until it meets the Bulla and eats it.  Note that in its passage the predator passes within about 1-2cm of the resting Bulla, yet doesn’t sense it.  Paine 1963 Veliger 6: 1. Photos courtesy Kevin Lee, Fullerton, California diverkevin.

The use of contact chemoreception in prey-location by Navanax inermis is confirmed in another study in southern California in which the authors tether Navanax and watch which way the they attempt to turn when stimulated on various parts of the front of the body.  There are 3 structures at the front of the body that potentially mediate predatory responses (see drawing upper Right).  These are the anterior lateral folds, tentacles, and the pharyngeal lips of the pharynx. The lips are generally hidden, but become exposed when the pharynx is protracted (extended). 

Stimuli used include cotton swabs, both clean (control) and soaked in mucus of Hermissenda crassicornis, and live Hermissenda or pieces of Hermissenda. Application of mucus or fresh pieces of Hermissenda to one or other lateral folds stimulates Navanax to turn in that direction (96%) versus a lesser response to control swabs (28%).  Contact appears to be necessary, as mucus-soaked swabs held near the lateral folds elicit no response. In comparison with the 96% value for the lateral folds, application of mucous swabs to the tentacles produces only 25% turning.  Application of live Hermissenda (or fresh pieces) to the tentacles causes 100% turning.  When live prey is touched to the pharyngeal lips, the pharynx begins to suck.  The authors conclude that sensors on the anterior lateral folds are responsible for trail recognition and that they respond only to contact, not to water-borne, stimuli.  Thus, when Navanax encounters a prey trail it turns onto the trail and any deviation from the trail is auto-corrected by asymmetrical stimulation of the lateral folds. 

The sensory units on the lateral folds and tentacles appear to be small ciliary tufts that the authors call phalliform organs.  There are about 1000 of these 0.5mm-sized units scattered over the combined surfaces of the lateral folds and tentacles.  The tufts are retractable (for protection?) and each is associated with a ganglion within the base of the tuft.  The study raises many good research questions, including the chemical identity of the stimulus, how it is recognised by the ciliary tufts, and how Navanax identifies the direction of the trail when it first encounters it. courtesy Kevin Lee, Fullerton, California. Photo of head of Navanax inermis courtesy Kevin Lee, Fullerton, California diverkevin..

NOTE  the difference noted here is statistically significant, but should be viewed with caution as repeated tests are made on a few individual Navanax and the data analysed as though they are independent (58 tests on 6 test specimens)

NOTE  lit. “penis shape” L.

Despite all of these confirmations that distance chemoreceptive ability is lacking in Navanax inermis, a later laboratory study suggests that there may, in fact, be such an ability.  The authors use a T-maze to assess the ability of Navanax to locate prey Bulla goldiana, another cehalaspidean, from a distance.  The results are not overwhelming, but a significant proportion of Navanax (62%) select the prey-containing arm of the maze over the empty arm (38%).  In addition, when exposed to seawater bearing the scent of the prey, Navanax exhibits increased locomotory movements.  Susswein et al. 1982 Mar Behav Physiol 8: 231.

NOTE  another research group reports the discovery of 2 identical polypropionates in Navanax inermis and Bulla gouldiana, thus providing a possible chemical basis for the predator-prey relationship.  Spinella et al. 1993 Tetrahedron 49: 3203.

NOTE  the authors use 3 runs of 18 specimens to yield 54 data points, so pseudoreplication is involved; therefore, the authors’ interpretation of their results should be viewed with caution

In Santa Catalina Island, California the opisthobranch-eating cephalaspid Navanax inermis attacks and consumes sea hares Aplysia californica.  In the field, Navanax prefers Aplysia of lengths greater than about 2cm.  However, at lengths greater than about 10cm, Aplysia reaches a refuge in size.  If the predator attempts to swallow a larger-sized prey, it is usually rejected.  In some cases, a large Aplysia may get stuck in Navanax's gullet for several minutes or hours, leading to partial digestion.  Survival of these damaged Aplysia often depends upon the extent to which gas exchange via the ctenidia has been impeded. Laboratory experiments indicate that the probability of successful attack by Navanax on Aplysia depends upon their relative sizes (see graph on Left). Note in the graph that if the predator is more than twice the length of the prey, then the probability of success is 60-100%.  As the two get closer in size, however, attack success falls off to 20% or less.  If cover, such as tufts of red algae Plocamium cartilagineum is provided in the test aquaria, then encounter frequencies decrease significantly, especially for the smaller size-classes of prey.  Pennings 1990 Mar Ecol Progr Ser 62: 95.

Onchidoris

Peltodoris

In the San Diego area of California Peltodoris (Anisodoris) nobilis eats several species of sponges, most notably Myxilla agennes.  McBeth 1971 Veliger 14: 158.

Radular characteristics such as number of cusp rows, number of cusps per row, and length of cusps are often used in taxonomic studies to differentiate species.  However, a study at Friday Harbor Laboratories, Washington of these features in Peltodoris (Anisodoris) nobilis (photo on Left) and Doris montereyensis (photo on Right), two large-sized spongivorous nudibranchs, show that while all 3 features change significantly with increasing live mass, as expected, the 2 species cannot be differentiated on the basis of radular characteristics.  The authors argue that radular characteristics are of little taxonomic use in this group of molluscs; specifically, regression statistics of radular characters would be of limited utility in delineating species unless live mass is taken into account, and then only for number of cusp rows and length of cusps.  As for the latter, the data¹ do show a significant difference in the relationship of increasing cusp size to increasing live mass in the two species, with Doris² maintaining relatively shorter cusps with increasing body size.  This is interpreted as a progressive “fine-tuning” of the species’ resource-utilisation abilities.  Doris feeds on sponges with little or no skeletal organisation.  Thus, an increase in food intake with increasing body size can be realised with a simple increase in number of rows and number of cusps per row, with the cusps remaining relatively short³.  In contrast, Anisodoris feeds on sponges with highly organised and robust skeletons.  Here, a longer relative tooth size with increasing body size will maximise the amount of prey ingested per unit time.  Bloom & Bloom 1977 J Moll Stud 43: 296.

NOTE¹ the authors have chosen to present all their data as tabulated regression statistics, which is fine for the science part of the study, but falls short on clarity of presentation

NOTE² cusp size in Peltodoris increases with body mass at about 4 times the rate of increase in Doris

NOTE³ the authors provide an apt analogy of boosting the size of a “broom” while maintaining a constant “bristle” size

Phidiana

The aeolid nudibranch Phidiana hiltoni in California usually preys on hydroids, but recent work by researchers at the Marine Sciences Institute, Santa Barbara shows that it will also eat several species of nudibranchs.  This is shown directly by diet analyses and laboratory feeding trials, and indirectly by effects on nudibranch populations in areas of northrn California into which P. hiltoni is spreading.  The movement northwards from the species’ previously most northerly limit of distribution is shown on the maps above dating from 1904.  Through feeding tests in the laboratory the researchers determine which other nudibranch species are vulnerable to predation by Phidiana, then they correlate this vulnerability with the extent to which these other nudibranch species have increased or decreased in numbers after the arrival of P. hiltoni (see histogram below Right). Of 40 nudibranch species observed, 15 are found to be vulnerable (including P. hiltoni itself) and these have shown a statistically significant two-thirds decline in overall population numbers over the 3-decade span between assessments.  In comparison, 25 non-vulnerable species exhibit no significant overall change in numbers.  Only P. hiltoni has significantly increased in number.  The authors conclude that the incursion of P. hiltoni has likely caused the decline, perhaps through a combination of predation and competition for hydroid prey.  The causes for range expansion of P. hiltoni may relate to warming coastal water temperatures in that part of California.  Goddard et al. 2011 Mar Biol 158: 1095. Photograph courtesy Kevin Lee, Fullerton, California diverkevin.

NOTE¹   overall, 20 taxa are present in feces of 62 field-collected P. hiltoni.  Eight of these taxa are hydroids, and these represent over 80% of the prey records.  Genus Plumularia is the most common hydroid prey

NOTE²  population numbers of nudibranchs are assessed by timed counts during 1969-1975 and again in 2007-2009.  Literature reports yield distributional data for P. hiltoni for dates outside of the authors’ own collections, during the period 1904-2010

NOTE³  while this is true for overall nudibranch numbers, only 2 species, Hermissenda crassicornis and Cuthona albocrusta, show significant decreases in population numbers. It also should be noted that 4 non-vulnerable species also decline significantly in numbers during the same period

Phidiana hiltoni 6X

Phyllaplysia

Phyllaplysia taylori inhabits eelgrass plants Zostera marina and eats mainly diatoms growing on the blades of the eelgrass. Diatoms have a tough, siliceous outer covering and are generally abrasive to soft tissues.  Phyllaplysia’s radula is broad with evenly spaced shovel-shaped cusps. The food is scraped up with the radula and passed through a pair of jaws made of numerous tightly packed small rods, and is moved into the esophagus. From the esophagus the food goes to a small crop. Paired salivary glands provide mucus for lubrication and possibly some enzymes for preliminary digestion. 

From the crop the food goes to a gizzard-like stomach, which is a large muscular sac lined with intermeshing chitinous teeth that grind the diatoms to a paste (see drawing on Right).  The food then moves through the posterior gizzard and is strained through a dozen or so long spines that project from the wall of the gizzard. Final digestion and absorption occur in the digestive gland.

Studies on Phyllaplysia from Elkhorn Slough, California in which stomach teeth are stained by brief exposure to a radioactive label show that 4% of each tooth is replaced by growth every day.  Replacement of a tooth in 25d far exceeds the normal wear from a diet of diatoms and the author suggests that the excess is worn off by the milling action of the intermeshing motion of the teeth.  Beeman 1969 Biol Bull 136: 141; drawing of Phyllaplysia from Beeman 1970 Veliger 13: 1; drawing of gut system from McCauley 1960 Proc Cal Acad Sci 29: 549.

NOTE an injection of 3µc of H3-thymidine per gram live body mass.  This produces a distinct labelled band at the base of each stomach tooth within 10h.  The subsequent movement of the band up to the grinding tip
of the tooth is followed autoradiographically over the next 25d

Radular cusps of Phyllaplysia taylori

Pleurobranchaea

The large notaspidean Pleurobranchaea californica is an active predator and scavenger.  It finds its food through perception of odours and will follow a scent down a chemical gradient. Tests using application of squid juice to various parts of the body show that the sensitive areas to food odours are concentrated on the anterior parts of the oral veil and foot, and the tips of the rhinophores (indicated by purple dots on the drawings).  Pleurobranchaea can readily track prey located in the arms of T-mazes.  Lee et al. 1974 Behav Biol 12: 297. Photo courtesey John Butler, La Jolla, California and NOAA

Mating Pleurobranchaea californica at 265m
depth off the coast of San Diego, California.

Pleurobranchaea californica has been the subject of many learning and behavioural studies.  Its repertoire of behaviours, including crawling, egg laying, copulation, swimming, and feeding are organised hierarchically, with feeding occupying a relatively dominant position.  Feeding involves quick eversion of a proboscis that grasps, ingests, and swallows food consisting of various living and dead organisms.  The dominance of feeding behaviour is illustrated when an indivual is flipped onto its back.  Normally, righting occurs within a few seconds but, if pieces of raw squid are fed to an inverted indivual, it remains on its back until feeding is completed.  There is plasticity in this dominance hierarchy.  For example, when an individual is laying eggs, feeding is suppressed, thought by the authors to be possibly an adaptation to reduce the risk of an individual consuming its own eggs.  If hemolymph from  an egg-laying individual is injected into a non-laying one, both egg-laying and suppressed-feeding behaviours are induced, suggesting that the behaviours are hormonally regulated.  The researchers are able to modify behaviours through a form of learning known as classical conditioning, as follows. 

Later, the same individual can be re-trained to exhibit the classical conditioning response more quickly than can naïve animals, signifying memory retention.  From these and many other pioneering experiments in the mid 1960s-early 1970s on Pleurobranchaea and other opisthobranch species, has arisen a large research discipline on brain, behaviour, and neurophysiology of learning that continues to present day.  Davis et al. 1974 Am Zool 14: 1037; see also Davis et al. 1977 J Comp Physiol 117: 99.

NOTE  for example, 20 over a 1-h period

NOTE a plethora of learning studies exists for several west-coast species of opisthobranchs, including P. californica, Hermissenda crassicornis, Tritonia spp.and Aplysia californica.  As these are outside of the intended scope of the ODYSSEY, other than this brief mention here the subject won’t be considered further