Pernet Lab - Publications

For electronic reprints of these papers, please contact me (bpernet@csulb.edu), and for a more compact list, see my CV.

PEER-REVIEWED JOURNAL ARTICLES
(#=CSULB graduate student coauthor, *=CSULB undergraduate coauthor)
20) Pernet, B., A. Deconinck*, and L. Haney. In press. Molecular and morphological markers for distinguishing the sympatric intertidal ghost shrimps Neotrypaea californiensis and N. gigas in the Eastern Pacific. Journal of Crustacean Biology.
The vigorous burrowing activities of many thalassinidean shrimp have such dramatic effects on their soft sediment habitats that these animals are often considered exosystem engineers. Because they are strong interactors in these communities, basic information about their life histories and population dynamics is needed to effectively manage the habitats in which they live. These data can only be obtained if the shrimp can be accurately identified. On the west coast of the United States, two species of burrowing intertidal shrimp in the genus Neotrypaea, N. californiensis and N. gigas, often co-occur and are not easily differentiated morphologically except as adult males by characters of the major claw (which is often lost in collection). Here we describe and validate (using mtDNA data from the cytochrome b gene) an allozyme marker (LDH) that can be scored rapidly and inexpensively for the identification of these species. We used this marker to generate a large sample of molecularly-identified specimens that we then used to evaluate a variety of morphological characters in an effort to differentiate the two species. With the exception of characters associated with the male major claw, most of the morphological characters examined here were not useful in distinguishing members of the two species. The exceptions were two simple and robust characters associated with the eyestalks -- length, and shape of the distal outer edges. These could be used to reliably differentiate between the two species regardless of sex and over a wide range of sizes. We hope that these characters will facilitate future studies of the distribution, habitat preference, and comparative biology of the two often co-occurring species.

19) Sloan, L.*, S. Anderson*, and B. Pernet. In press. Kilometer-scale spatial variation in the prevalence of the the rhizocephalan Lernaeodiscus porcellanae on the porcelain crab Petrolisthes cabrilloi. Journal of Crustacean Biology.
We studied spatial variation in the prevalence of the rhizocephalan barnacle Lernaeodiscus porcellanae on its porcelain crab host, Petrolisthes cabrilloi, at four southern California intertidal sites separated by only a few km. The prevalence of rhizocephalan externae varied significantly among sites in 2008-09, with the southernmost site, White Point, consistently showing higher prevalence than the others. Externa prevalence was a good proxy of estimated true prevalence (i.e., the prevalence of rhizocephalans as a whole, not just those that had formed externae). We examined several hypotheses that might explain the observed spatial variation in prevalence. Host susceptibility to infection (indicated by the proxy of damage to host limbs, some of which are used to remove parasite infective stages) did not differ among sites. At all sites, prevalence was slightly higher in female crabs than in males, and the sex ratio at White Point was slightly female-biased while that at the other sites was male-biased; thus, among-site differences in sex ratio did contribute to the observed variation in prevalence. However, most spatial variation in prevalence appeared to be due to the effect of host size. At all sites the probability of infection increased with increasing host size, and White Point crabs were on average much larger than crabs at other sites. Overall, the size-class distribution of host crabs explained 80.4% of the variation in prevalence of L. porcellanae. Larger P. cabrilloi have likely had greater opportunity to be infected by rhizocephalans, either because they are older, or because they have undergone more molts (during which they are especially vulnerable to infection). A deeper understanding of small-scale spatial variation in prevalence in L. porcellanae will require information on the causes of among-site variation in host population size structure.

18) Kosman, E.# and B. Pernet. In press, 2009. Diel variation in the sizes of Bugula neritina larvae in field populations. Biological Bulletin.
The scale of planktonic larval dispersal affects a variety of ecological and evolutionary processes. Recent work suggests that the dispersal ability of obligately lecithotrophic larvae is influenced by the amount of energy supplied to each larva: largers larvae may stay in the plankton longer and thus travel greater distances than smaller larvae. We examined a prediction of this hypothesis in the bryozoan Bugula neritina, which each morning releases brooded larvae that settle within a few hours. If larger larvae stay in the plankton longer than smaller larvae, then larger larvae should increase in frequency in the planktonic population as the day progresses. However, field surveys revealed a negative relationship between time of day and the sizes of planktonic larvae. As these results may have been complicated by prolonged larval release, we sequestered groups of brooding colonies in field mesocosms to examine release patterns. Larvae were released over a period of 8-9 hours, with smaller larvae increasing in frequency as the day progresses. We conclude that populations of larvae of B. neritina may not be homogeneous in energetic content throughout the day; this must be taken into consideration when designing studies of many aspects of larval biology.

17) Pernet, B., A. Deconinck*, A. Llaban*, and J. Archie. 2008. Evaluating risks associated with the transport of the ghost shrimp Neotrypaea californiensis as live bait. Marine Biology 153:1127-1140.
The ghost shrimp Neotrypaea californiensis is imported into southern California from Oregon and Washington for use as live bait in recreational marine fisheries.   We studied the population genetic structure of N. californiensis across much its range to assess the possibility that the transport of ghost shrimp across phylogeographic boundaries poses a risk of homogenizing existing genetic variation in the species.   Analyses of two mitochondrial DNA markers showed little phylogeographic structure across the sampled range, suggesting that this risk is low.   Unexpectedly, mitochondrial DNA analyses revealed that a second putative species of ghost shrimp frequently coexisted with N. californiensis in southern California intertidal habitats; almost all previous studies of soft-sediment communities in the region report the presence of N. californiensis only.   We also assessed the possibility that the import of ghost shrimp might pose a risk of introduction of a parasitic castrator, the bopyrid isopod Ione cornuta , into southern California waters, where it does not appear to be native.   Prevalence of living I. cornuta in samples purchased from bait shops was high (5.8%), suggesting that this is a real risk that merits further study.

16) Allen, J. and B. Pernet. 2007. Intermediate modes of larval development: bridging the gap between planktotrophy and lecithotrophy. Evolution and Development 9:643-653.
The extraordinary diversity of larval form and function in marine invertebrates has motivated many studies of development, ecology and evolution. Among organisms with pelagic development via a larval stage, this diversity is often reduced to a dichotomy between two broad nutritional strategies: planktotrophy and lecithotrophy. Despite the clear utility of the planktotrophy-lecithotrophy dichotomy to those interested in the history or consequences of life history patterns, it is also clear that a number of larval forms do not fit neatly into either of these general categories. Here we review studies of these intermediate larval forms, focusing on descriptions of larvae known as facultative feeders. Recent descriptions of larval development suggest that facultative feeders and other intermediate larval forms are not as rare as commonly assumed. We assess the importance of these forms for models of life history evolution and call for a more detailed and nuanced view of larval biology to account for their existence. Clearer knowledge of the phylogenetic distribution and frequency of occurrence of larvae that use intermediate nutritional strategies is also essential for evaluating current ideas on evolutionary transitions between planktotrophy and lecithotrophy.   Finally, intermediate larval types provide valuable and underutilized opportunities for testing hypotheses in the fields of larval ecology and the evolution of development.

15) Pernet, B. 2007. Determinate growth and variable size at maturity in the marine gastropod Amphissa columbiana. American Malacological Bulletin 22:7-15.
Amphissa columbiana from the intertidal zone of San Juan Island, Washington, USA, typically have either shells with very thin, delicate apertural lips, or shells with thick, robust lips.   In laboratory observations, thin-lipped snails grew rapidly but were not sexually mature, while thick-lipped snails grew very slowly or not at all and were sexually mature.   These observations are consistent with the hypothesis that A. columbiana displays determinate growth, as has been inferred for many columbellids on the basis of intraspecific variation in shell form.   Sizes of mature snails were very variable, with the largest individuals weighing 4.5 times more than the smallest (wet weight, excluding shell).   I tested the hypothesis that maturation and associated shell thickening are phenotypically plastic responses to the presence of predators.   Exposure to effluent from the predatory crab Cancer productus in the laboratory had no effect on shell form or relative shell weight (an index of shell thickness), suggesting that this is not the case.

14) Pernet, B. and L. McArthur*. 2006. Feeding by larvae of two different developmental modes in Streblospio benedicti (Polychaeta, Spionidae). Marine Biology 149:803-811.
Females of the spionid polychaete Streblospio benedicti (Webster) produce either small eggs (60-70 µm diameter) and planktotrophic larvae, or large eggs (100-200 µm) and lecithotrophic larvae that reportedly do not feed.   This intraspecific polymorphism, a form of poecilogony, is potentially useful in studies of larval ecology and evolution, but necessary data on larval form and function are lacking.   This study describes the morphology and nutritional biology of larvae obtained from Atlantic (South Carolina) and Pacific (California and Washington) populations from 2003-2005.   The two types of larvae produced by Atlantic S. benedicti differed greatly in length (229 ± 22 µm SD for planktotrophs vs 638 ± 40 µm for lecithotrophs) and chaetiger number (2-5 vs 10-11) at release from the female's brood pouch.   Planktotrophic larvae bore long provisional chaetae on their first chaetiger; provisional chaetae were absent in lecithotrophic larvae.   Larvae from Pacific populations were all of the lecithotrophic form, and were similar to their Atlantic counterparts in all respects.   High-speed video microscopy revealed that both types of larvae used opposed bands of cilia to capture suspended particles and transport them to the mouth, where they were often ingested.   Lecithotrophic larvae reared with suspended phytoplankton (Rhodomonas sp., 10,000 cells per ml) for 2 d grew significantly faster than sibling larvae reared without added food, indicating that these larvae can digest and assimilate ingested food.   Larvae of S. benedicti that develop from large eggs are thus facultative planktotrophs instead of obligately non-feeding lecithotrophs, a result that affects the interpretation of comparative studies of the ecology and evolution of larvae in S. benedicti and certain other marine invertebrates.

13) Pernet, B. 2004. The cryptic filtering house of an invertebrate larva. Science 306:1757.
The minute and diverse feeding larvae of marine invertebrates typically concentrate suspended food particles on complex arrays of cilia or setae. Here I show that the planktonic larvae of an annelid worm use a very different strategy: building large, transparent "houses" through which they filter seawater to concentrate food. This feeding mechanism is unlike any previously described in marine larvae but is strikingly similar to that of the very distantly related larvacean chordates. Cryptic and ephemeral secreted structures like these may be involved in the performance of critical functions in many marine invertebrate larvae, which would have important implications for our understanding of their ecology and evolution. [The cartoon above is from a very brief story about this work published in the 7 Dec 04 New York Times.]

12) Pernet, B. and W.B. Jaeckle. 2004. Size and organic content of eggs of marine annelids, and the underestimation of egg energy content by dichromate oxidation. Biological Bulletin 207:67-71.
Dichromate oxidation is a simple technique that is often used to estimate the energy content of eggs in studies of marine invertebrate life histories.  We used this method to measure energy contents of eggs of 12 species of marine annelids.  In combination with measures of egg ash-free dry weight (AFDW), these data yielded estimates of AFDW-specific energy density that were mostly lower than the average weight-specific energy density of carbohydrates.  This seemed unlikely to be correct, as invertebrate eggs typically contain little carbohydrate and instead are composed primarily of energy-dense protein and lipid.  After validating our methods (by using them to estimate energy content and AFDW of the eggs of a previously studied echinoderm) and reexamining published data on the energy contents of echinoderm eggs, we conclude that dichromate oxidation often underestimates the energy contents of small eggs of marine invertebrates.  This systematic error, which is likely related to the tendency of the assay to incompletely oxidize proteins, can only be corrected with substantial independent data on egg biochemical composition.  We thus suggest that dichromate oxidation should not be used for routine measurement of total egg energy content in marine invertebrates.

11) Pernet, B. 2003. Persistent ancestral feeding structures in nonfeeding annelid larvae. Biological Bulletin 205:295-307.
Evolutionary loss of the requirement for feeding in larvae of marine invertebrates is often followed by loss of structures involved in capturing and digesting food. Studies of echinoderms suggest that larval form evolves rapidly in response to loss of the requirement for feeding, but a lack of data from other taxa makes it difficult to assess the generality of this result. I show that many members of a large clade of annelids, the Sabellidae, retain ancestral particle capture systems despite loss of the need and ability to feed. In at least one species, Schizobranchia insignis, an opposed band system of prototrochal, food groove, and metatrochal ciliary bands can concentrate suspended particles and transport them to the mouth, but captured particles are invariably rejected because larvae lack a functional gut. The persistence of particle capture systems in larvae of sabellids suggests that they have lost larval feeding very recently, that opposed bands are inexpensive to construct and operate, or that opposed bands have some alternative function. These observations also suggest an hypothesis on how the ability to feed is lost in larvae of annelids and other spiralians following increases in egg size.

10) Pernet, B. 2001. Escape hatches for the clonal offspring of serpulid polychaetes. Biological Bulletin 200:107-117.
Serpulid polychaetes in the genera Filograna and Salmacina reproduce asexually by releasing a single bud at a time from their posterior ends into their calcareous tubes. Here I show that buds of Salmacina amphidentata gain access to the exterior of these tubes via escape hatches built into the tubes by the parent worms. Each escape hatch consists of a hole in the tube blocked by a calcareous disc which is supported in place by an organic membrane. After buds detach from their parents, the calcareous discs are dislodged and buds begin to form their own tubes from the resulting openings. Repeated bouts of asexual reproduction result in the formation of aggregations of branched tubes. A survey of Filograna and Salmacina spp. from the Atlantic, Indian, and Pacific Oceans suggests that the formation of escape hatches for clonal offspring is common to many members of these genera.

9) Pernet, B. 2000. A scaleworm's setal snorkel. Invertebrate Biology 119:147-151.
Setae of the first segment of the marine annelid Sthenelais berkeleyi (family Sigalionidae) are arranged in the shape of an antero-dorsally directed tube. When the worm is in resting position buried in sediment, this setal tube projects slightly from the sediment surface. A current of water is drawn into it by cilia on the parapodia of the first segment. The water is then diverted to a pair of lateral spaces between the body wall and elytra, moved posteriorly in these spaces along the length of the body by segmental cilia, and eventually exits posteriorly or ventrally. This flow permits the worm to respire while remaining buried and immobile for long periods of time, waiting for prey to move over the sediment near it. Setae of the first segment are probably used as snorkels in some other infaunal sigalionids as well.

8) Pernet, B. 2000. Reproduction and development of three symbiotic scaleworms (Polychaeta: Polynoidae). Invertebrate Biology 119:45-57.
The reproduction and development of symbiotic polynoid polychaetes in the genus Arctonoe was examined with light and electron microscopy. Around San Juan Island, Washington, the three described Arctonoe spp. have very similar reproductive periods and ontogenies. Free-spawned eggs 80 µm in diameter fuse with sperm and develop into planktonic, feeding larvae that bear a prototroch, but no metatroch or food groove cilia. Larvae begin feeding only after the development of episphere ciliary bands and an oral brush, consistent with the hypothesis that these structures are involved in particle capture and handling. Metamorphosis occurs in the laboratory in the absence of hosts after 6--12 weeks of feeding and growth. Juveniles begin feeding using the pharyngeal jaws several days after metamorphosis is complete. In the laboratory, worms reach sexual maturity 4-6 months after metamorphosis. The long planktonic larval period of Arctonoe spp. probably leads to high dispersal, suggesting that geographic differentiation in host preferences is unlikely except over very large spatial scales. Naive juveniles of Arctonoe spp. can now be obtained from laboratory cultures to test the hypothesis that genetically based host preferences are important in determining host-use patterns in these symbionts.

7) Kohn, A.J., M. Nishi, and B. Pernet. 1999. Snail spears and scimitars: a character analysis of Conus radular teeth. Journal of Molluscan Studies 65:461-481.
Knowledge of the attributes of the venom-injecting adular teeth of Conus can enhance understanding of the functional biology of feeding and the systematics of this large and taxonomically difficult genus of gastropods. We define and provide a scheme for coding the states of Conus radular teooth characters, in order to facilitate their use in taxonomic and phylogenetic studies. To exemplify these characters, we describe and illustrate teeth of putatively primitive species and of species representing generalized, vermivorous, molluscivorous, and piscivorous groups within the genus. We define and address the intraspecific and interspecific variation of ten presence-absence characters and 15 continuous characters, of which at least five and ten, respectively, are present in most species. Some continuous characters are bimodally distributed among the species sampled. If this distribution still obtains when additional species are examined, these characters could also be coded unambiguously as having two states. We also review the several previously proposed classification schemes of Conus radular teeth and of species according to tooth characteristers. As Troschel suggested in 1866, a tooth length:width ratio greater than or less than 20 separates the genus into two distinct species groups, now known to comprise the molluscivorous and piscivorous species in the former, and vermivorous and generalized species in the latter. Important subsidiary characters are the number of barbs, presence/absence of blade, cusp, and spur, length of serrations, relative width of base, and tooth length:shell length ratio.

6) Pernet, B. 1999. Gamete interactions and genetic differentiation among three sympatric polychaetes. Evolution 53:435-446.
The evolution of gamete incompatibility between free-spawning marine invertebrate species has been explained by three hypotheses: (1) independent divergence at gamete recognition loci, (2) selection against hybrids, and (3) a process of sexual selection involving polymorphic gamete recognition loci (Metz and Palumbi 1996). The first two hypotheses predict that gamete incompatibility appears only after gene flow has been halted for other reasons, and the third that gamete incompatibility appears simultanously with blocks to gene flow. Here I show that gametes of three sympatric polychaetes in the genus Arctonoe are compatible in all crosses, over a broad range of gamete concentrations and contact times. Though at least some hybrid crosses produce fertile adults, allozyme and mitochondrial DNA sequence data indicate that the three species do not regularly exchange genes. These data are consistent with predictions of the first two hypotheses for the evolution of gamete incompatibility, but allow rejection of the third hypothesis. Gametes of the three species are compatible despite estimated divergence times of 1-3 million years before present; in several other marine invertebrates, divergence times of the same magnitude are associated with asymmetric or complete gamete incompatibility. It appears likely that segregation of symbiotic adults on their respective host species restricts mating opportunities, and thus gene flow, among Arctonoe spp.

5) Miner, B., E. Sanford, R.R. Strathmann, B. Pernet, and R. Emlet. 1999. Functional and evolutionary implications of opposed bands, big mouths, and extensive oral ciliation in larval opheliids and echiurids. Biological Bulletin 197:14-25.
Larvae of two annelids, the opheliid Armandia brevis and the echiurid Urechis caupo, captured small particles between opposed prototrochal and metatrochal ciliary bands and also captured large particles with wide ciliated mouths. The body volume of larval A. brevis increased more rapidly than the estimated maximum clearance rate as segments were added. Capture of larger particles by late-stage larvae may compensate for this potentially unfavorable allometry. The existence of larvae that use two feeding mechanisms at once, not previously known in annelids, suggests possible evolutionary routes between larval forms that feed only with opposed bands (e.g., serpulids and oweniids) and those that use complex oral ciliature to feed primarily on large particles (e.g., polynoids and nephtyids). In particular, the metatroch and food groove of opposed-band feeders may have arisen as expansions of oral ciliation in ancestral large-particle feeders; alternatively, extensive oral ciliation in large-particle feeders may have originated as a modification of metatroch and food-groove cilia in ancestral opposed-band feeders.

4) Pernet, B. 1998. Benthic egg masses and larval development of Amblyosyllis speciosa (Polychaeta: Syllidae). Journal of the Marine Biological Association of the United Kingdom 78:1369-1372.
Eggs of the syllid polychaete Amblyosyllis speciosa Izuka, 1912, are deposited in benthic gelatinous masses. Embryos and larvae develop within these masses until about three weeks after fertilization, after which they crawl or swim away and metamorphose. Only one other syllid, the Mediterranean Syllides edentula Claparède, has been reported to form benthic egg masses.

3) Pernet, B. and A.J. Kohn. 1998. Size-related obligate and facultative parasitism in the marine gastropod Trichotropis cancellata. Biological Bulletin 195:349-356.
The marine gastropod Trichotropis cancellata, previously considered to be exclusively a suspension feeder, is also a kleptoparasite, stealing food from several species of suspension-feeding polychaetes. When feeding independently, T. cancellata uses its pseudoproboscis, an elongate, ciliated extension of the lower lip, to transport particles captured on its ctenidium to its mouth. When parasitizing, the snail positions its pseudoproboscis in the mouth of a host polychaete and diverts a large proportion of the particles captured by the polychaete to the its own mouth. In subtidal habitats around San Juan Island, Washington, most individuals of T. cancellata are found in association with the tube openings of suspension-feeding polychaetes. In laboratory experiments, parasitism significantly enhanced fitness in T. cancellata. Juvenile snails that parasitized polychaetes grew faster and survived in greater numbers than those deprived of access to hosts, and parasitic adult snails reproduced more than those without hosts. Parasitism in T. cancellata and related capulid gastropods may have originated in early post-metamorphic stages as a response to constraints on the efficiency of suspension feeding at small sizes; however, because parasitism is more effective than suspension feeding for snails of all sizes, it now persists throughout life.

2) Pernet, B. 1997. Development of the keyhole and growth rate in Diodora aspera (Gastropoda: Fissurellidae). Veliger 40:77-83.
Scanning electron micrographs of shells of the fissurellid Diodora aspera (Rathke, 1833) show that the apical opening, or keyhole, begins development as a shallow notch in the anterior edge of the aperture. This notch deepens as the adjacent shell grows until finally it is closed off, forming a complete subapical keyhole. As the animal grows, enlargement of the keyhole by shell dissolution eventually results in its placement at the shell apex. Observations of the growth of marked individuals in an intertidal population, and of laboratory-raised juveniles, suggest that D. aspera grow from settling to 55 mm aperture length in about 9-13 yr; thereafter, shell growth is even slower. The ages of large (60 mm or greater) snails may be in excess of 20 yr

1) Phillips, N.E. and B. Pernet. 1996. Capture of large particles by suspension feeding scaleworm larvae (Polychaeta: Polynoidae). Biological Bulletin 191:199-208.
Planktotrophic larvae of polynoid polychaetes lack a metatroch and food groove, and have a bundle of long cilia (the oral brush) attached to the left side of the prototroch. Feeding experiments and videotaped observations of larvae of the polynoid Arctonoe vittata showed that they feed in a manner unlike the more familiar opposed-band feeding polychaete trochophores, which capture particles with the prototroch and metatroch and transport them to the mouth via the food groove. In experiments with polystyrene beads and plankton, larvae of A. vittata ingested particles much larger (up to 60 µm in diameter) than those typically ingested by opposed-band feeders. In contrast, the opposed-band feeding larvae of Serpula vermicularis only ingested particles 12 µm or less in diameter. Videotaped sequences of feeding A. vittata larvae showed that capture behavior was elicited as particles in a feeding current driven by the prototroch approached or contacted the larval episphere. Particles on or very near the episphere were disengaged by a recoiling motion of the larva and were then moved to the mouth, probably by the oral brush. This feeding mechanism may be widespread in the polychaete superfamily Aphroditacea, which includes about 10% of extant polychaete species.

BOOK CHAPTERS, BOOK REVIEWS, ETC.
Pernet, B. 2004. An inordinate fondness for shrimps.   Review of R.T. Bauer , Remarkable shrimps: adaptations and natural history of the Carideans .   Ecology 85:3448.

Pernet, B. 2002. Sponge and Brachiopod entries in N. Eldredge, ed., Life on Earth: An Encyclopedia of Biodiversity, Ecology, and Evolution . ABC-CLIO, Santa Barbara.

Pernet, B., P.-Y. Qian, G.W. Rouse, C.M. Young, and K.J. Eckelbarger. 2002. Phylum Annelida: Polychaeta.   Pp. 209-243 in Young, C.M., ed., Atlas of Marine Invertebrate Larvae. Academic Press, London.

Pernet, B. Review of A.W.C. Dorresteijn and W. Westheide, eds., Reproductive strategies and developmental patterns in annelids. American Zoologist 40:453-454.

Last modified 23 Jan 2009