ArticlePDF Available

Factors Affecting Gastropod Larval Development and Performance: A Systematic Review

Authors:

Abstract and Figures

The goal of this article was to use a systematic review of studies on the larval stages of gastropods reared to metamorphosis to determine whether there are general patterns for the effects of temperature, rearing density, and food availability on larval development and performance among species, major taxa, and modes of development. Most studies did not include sufficient metadata to be included in many of the analyses. For all analyses, there were differences among major groups of taxa in terms of response to the considered variables. Increased temperature was frequently correlated with decreased development time and increased growth but often not for the same taxa. Increased larval density was generally correlated with increased development time, but again, the patterns were not consistent across taxa. The most consistent pattern was the positive correlation between per capita food availability and larval growth. In all but two cases, patterns for the most studied species, Crepidula fornicata, were opposite those of other caenogastropods. This indicates that caution should be used when drawing general patterns among species based on studies of C. fornicata. Among lecithotrophs, the vetigastropod Haliotis rufescens was the most studied. In this case, patterns found for this species were similar to those for all other vetigastropods; however, few species outside the genus Haliotis have been studied. Increased temperature was associated with reduced survivorship and, in the most studied clade, the Vetigastropoda, reduced time to metamorphosis, which suggests that there may be an energetic cost to more rapid development or physiological mechanisms for coping with heat stress. Curiously, increased larval density was associated with increased survivorship for lecithotrophs. In several cases, however, there were too few studies, or the studies that were found did not provide enough metadata to be included in analyses. Although some patterns emerged from existing research on gastropod larvae, studies on a more diverse set of species that report all metadata are required for cross-study comparisons, which are crucial for drawing robust general conclusions. © 2018 National Shellfisheries Association. All rights reserved.
Content may be subject to copyright.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research
libraries, and research funders in the common goal of maximizing access to critical research.
Factors Affecting Gastropod Larval Development and Performance: A Systematic
Review
Author(s): Dianna K. Padilla, David Charifson, Alyssa Liguori, Mica McCarty-Glenn, Maria Rosa and
Allison Rugila
Source: Journal of Shellfish Research, 37(4):851-867.
Published By: National Shellfisheries Association
https://doi.org/10.2983/035.037.0414
URL: http://www.bioone.org/doi/full/10.2983/035.037.0414
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and
environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published
by nonprofit societies, associations, museums, institutions, and presses.
Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of
BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.
Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries
or rights and permissions requests should be directed to the individual publisher as copyright holder.
FACTORS AFFECTING GASTROPOD LARVAL DEVELOPMENT AND PERFORMANCE:
A SYSTEMATIC REVIEW
DIANNA K. PADILLA,*
DAVID CHARIFSON, ALYSSA LIGUORI, MICA MCCARTY-GLENN,
MARIA ROSA AND ALLISON RUGILA
Department of Ecology and Evolution, Stony Brook University, 650 Life Sciences, Stony Brook, NY
11794-5425
ABSTRACT The goal of this article was to use a systematic review of studies on the larval stages of gastropods reared to
metamorphosis to determine whether there are general patterns for the effects of temperature, rearing density, and food
availability on larval development and performance among species, major taxa, and modes of development. Most studies did not
include sufficient metadata to be included in many of the analyses. For all analyses, there were differences among major groups of
taxa in terms of response to the considered variables. Increased temperature was frequently correlated with decreased
development time and increased growth but often not for the same taxa. Increased larval density was generally correlated with
increased development time, but again, the patterns were not consistent across taxa. The most consistent pattern was the positive
correlation between per capita food availability and larval growth. In all but two cases, patterns for the most studied species,
Crepidula fornicata, were opposite those of other caenogastropods. This indicates that caution should be used when drawing
general patterns among species based on studies of C. fornicata. Among lecithotrophs, the vetigastropod Haliotis rufescens was
the most studied. In this case, patterns found for this species were similar to those for all other vetigastropods; however, few
species outside the genus Haliotis have been studied. Increased temperature was associated with reduced survivorship and, in the
most studied clade, the Vetigastropoda, reduced time to metamorphosis, which suggests that there may be an energetic cost to
more rapid development or physiological mechanisms for coping with heat stress. Curiously, increased larval density was
associated with increased survivorship for lecithotrophs. In several cases, however, there were too few studies, or the studies that
were found did not provide enough metadata to be included in analyses. Although some patterns emerged from existing research
on gastropod larvae, studies on a more diverse set of species that report all metadata are required for cross-study comparisons,
which are crucial for drawing robust general conclusions.
KEY WORDS: Crepidula fornicata,Haliotis, lecithotrophic development, planktotrophic development, veliger
INTRODUCTION
For most biological questions of interest, it is important to
know the generalizability of studies of individual species; can
a study on one species of mollusc, or even one species of
gastropod, be generalized to other, similar species? Much
biological research presently focuses on a few key model species.
Model species are selected for focused study because aspects of
their life history, development, or genetic characteristics make
them particularly amenable to experiments. In other cases,
species are selected for focused study because of economic or
other social importance to humans. But, as more information is
gained, even greater variation in many traits among and within
species has been found. Thus, an understanding of important
phylogenetic or evolutionary signatures that appear to drive
patterns among species, or correlations between species traits
and ecological or environmental conditions, are needed to make
the most of the data that exist and to focus future studies.
For studies on biological systems, particularly organismal
biology, new information on various aspects of individual
species appears continually. As a consequence, the ability to
digest this deluge of information poses a great challenge. To
date, however, the ability to generalize among species, or to find
general principles or patterns, is limited. Ultimately, there is
hope that studies of single species, including studies of early life
stages of invertebrates, can reveal general principles. For many
important questions in biology, this assumption remains
untested.
The first goal of this review was to examine studies on the
larval stages of gastropods and determine if there are patterns
among species, major taxa, and development modes in terms
of the effects of temperature and food availability on devel-
opment time and survivorship. A second goal was to determine
whether overall food concentration, independent of animal
density, or per capita food ration had a greater impact on
development time, in particular, time to metamorphosis as
well as survivorship during the larval phase for species with
planktotrophic larvae. These questions are important for
understanding potential trade-offs between physiological pro-
cesses during early life history stages, potential limits on wild
populations, and the relative importance of these factors for
growing animals in laboratory experiments and for aquacul-
ture. Therefore, a systematic review of the literature on
experiments conducted with gastropod larvae was used to
determine if patterns could be discerned from existing studies.
Systematic reviews are intended to be exhaustive reviews of
published literature focused on a particular research question
and include literature obtained through repeatable search
methods, allowing a synthesis of all high-quality research
evidence relevant to the question of interest (Pullin & Stewart
2006). The methodology used for a systematic review needs to
be transparent and repeatable so as to minimize the bias of
information included. This approach produces a survey of
a very broad range of literature, and not just a focus on
literature most familiar to the authors, or only the most
recently published studies.
*Corresponding author. E-mail: dianna.padilla@stonybrook.edu
All authors contributed equally to this paper.
DOI: 10.2983/035.037.0414
Journal of Shellfish Research, Vol. 37, No. 4, 851–867, 2018.
851
MATERIALS AND METHODS
To identify articles suitable for inclusion in this review,
a systematic review of the published literature was conducted.
First, the literature was searched through a number of web-
based literature collections and databases. In all cases, searches
included from January 1 of the earliest year available through
the Stony Brook University Library collection through
December 14, 2016. This included the Web-of-Science Core
Collection, which includes Science Citation Index Expanded
(1900 to present), Social Sciences Citation Index (1956 to
present), Arts and Humanities Citation Index (1975 to present),
Conference Proceedings Citation Index: Science (1991 to pres-
ent), Conference Proceedings Citation Index: Social Science and
Humanities (1991 to present), Book Citation Index: Science
(2005 to present), Book Citation Index: Social Sciences and
Humanities (2005 to present), Emerging Sources Citation Index
(2015 to present), Current Chemical Reactions (1985 to present,
which also includes Institut National de la Propriete Industri
ell
e
Structure Data back to 1840), and Index Chemicus (1993 to
present). Biological Abstracts (1980 to present), BIOSIS Citation
IndexSM (1926 to present), Current Contents Connect (1998 to
present), Data Citation IndexSM (1900 to present), Derwent
Innovations IndexSM (1963 to present), KCI-Korean Journal
Database (1980 to present), MEDLINE (1950 to present),
Russian Science Citation Index (2005 to present), SciELO
Citation Index (1997 to present), and Zoological Record (1864
to present) were also included in the search.
In all cases, the key words gastropod* AND larv* AND
experiment NOT Crepidula* NOT parasite were used. Articles
on the gastropod genus Crepidula (Lamarck, 1799) were found
for a previous project (Padilla et al. 2014) by using the search
terms larv* AND experiment AND Crepidula* NOT parasite
and were added to the literature discovered through this search.
Articles on Crepidula spp. larvae were then searched using the
same search terms to find articles published from the end of the
previous search (May 31, 2013) through December 16, 2016.
Initial searches yielded 558 citations, seven of which were
duplicates, six citations that were not on gastropods or did not
include experiments, plus an additional 113 publications on
Crepidula for a total of 671 publications. Attempts were made
to find experts to translate the articles that were not in English.
All but two articles in Korean and one article in Japanese were
translated. Publications that focused on embryos in egg cases or
masses, or studies that were nonexperimental observations of
a few individuals, and studies where animals were not identified
to species were not included. After close reading, 126 articles
had sufficient data and metadata and were included in this
review. Because some studies included multiple experiments and
multiple experimental treatments (e.g., different temperatures
or food concentrations), each experiment and experimental
treatment within each study were considered separately in the
review. For each study, the species that was the focus of the
study or experiment was determined. The World Register of
Marine Species was used to determine current taxonomic status
of accepted species and subspecies names as of January 19,
2018.
The following were determined for each species: the de-
velopmental mode (whether larvae were planktotrophic, lec-
ithotrophic, facultative planktotrophic, or poecilogonous),
major taxonomic clade, geographic range, habitat types
(e.g., subtidal or intertidal zone), and trophic type (detritivore,
herbivore, predator, scavenger, and suspension feeder). The
following were recorded (if reported) for each experiment in
each publication: larval density, microalgal food fed for feeding
larvae, food concentration, and feeding frequency. Also
recorded (if reported) were water change frequency, rearing
temperature, time to metamorphosis, time to competence,
survivorship, growth rate, and the time over which growth
was quantified. In some treatments of some experiments, larvae
were starved, and those cases were considered a food density of
zero. Studies that reported that larvae were fed ad libitum could
not be used when considering the density of food that larvae
were fed. For larval competence, only studies that experimen-
tally tested for competence and provided a percentage of larvae
that were competent for metamorphosis after a specific number
of days were included. For metamorphosis, only studies that
reported the time to metamorphosis were included. And, for
survivorship, only studies that provided a quantitative assess-
ment of survivorship were included.
Correlations among factors of interest were then tested,
including temperature, larval density, food concentration, and
per capita food availability.
RESULTS
A total of 126 publications were included in this review.
Experiments with planktotrophic larvae were the focus of 84
publications (67% of all publications) published from 1967 to
the present (Fig. 1). For species with lecithotrophic larvae, 46
articles (37% of the total) were included. The search results also
included seven publications on five species with poecilogony, all
of which are in the Heterobranchia clade. For poecilogonous
species, experiments and experimental treatments conducted on
planktotrophic larvae were considered with those from species
with planktotrophic development and larvae with lecithotrophy
considered with species that have lecithotrophic development.
These species included Alderia modesta (Lov
en, 1844) and
Alderia willowi (Krug, Ellingson, Burton & Vald
es, 2007)
(Seelemann 1967, Krug et al. 2012), which are herbivores,
whereas Dendronotus frondosus (Ascanius, 1774) (Sisson
2002), Tenellia adspersa (Nordmann, 1845), and Phestilla
sibogae (Bergh, 1905) are predators (Chester 1996). These five
species are evenly split between those that are subtidal, in-
tertidal, or both and are mostly from the Atlantic in North
America and Europe, but one species is from the Indo-Pacific.
For 38 species, there was only a single publication reporting
research on larval development to metamorphosis. Of those 38,
13 publications included a single experiment with only one
treatment. The rest had from 2 to 10 different treatments within
one experiment in a publication. The remaining publications
included from two to six experiments with up to 28 total
different treatment levels in the same publication (Table 1).
By far, the most publications were on species of Crepidula
(42 publications) and primarily on Crepidula fornicata
(Linnaeus, 1758) (33 publications, 82 different experiments,
and 281 cumulative different treatment levels), which has
planktotrophic larvae. The second most studied group was
the genus Haliotis (37 publications). All species in this genus
have lecithotrophic larvae. Twelve different species have been
studied, and Haliotis rufescens (Swainson, 1822) has been the
focus of most of these studies (12 publications, 18 experiments
PADILLA ET AL.852
with a total of 60 different treatments). The species Haliotis
diversicolor (Reeve, 1846) and Haliotis iris (Gmelin, 1791) were
each the focus of five publications. Studies of H. diversicolor
included 10 different experiments and 30 different treatment
levels and for H. iris, there were seven different experi-
ments with 15 different treatments. The third most studied
species was Lobatus (Strombus)gigas (Linnaeus, 1758), which
has planktotrophic larvae (eight publications, 12 different exper-
iments, and 62 different treatment levels). The remaining species
were the focus of from two to five publications, including from
2 to 12 total experiments and 2 to 40 total different treatment
levels (Table 1).
Planktotrophic Larvae
Studies on planktotrophic larvae included 36 currently
recognized species within 25 currently recognized genera (Table 1).
The larvae of one species, Conus pennaceus (Born, 1778), are
reported to be facultative planktotrophs (Perron 1981) and were
included with the planktotrophs. Studies with planktotrophic
larvae included 28 species of Caenogastropoda, 13 of which are
in the Neogastropoda, and eight species of Heterobranchia
(Table 1). In terms of trophic roles, two species were detri-
tivores, 11 species were herbivores, 13 were predators, four were
scavengers, which may also be predators or detritivores, and six
species were suspension feeders.
In terms of the major types of habitats, for species with
planktotrophic larvae, including the facultative planktotroph,
two species are found in brackish waters, and 15 species live in
the intertidal zone, whereas 13 species are primarily found in the
subtidal zone. Species that were the targets of study are from
a wide range of geographic areas, covering most of the globe,
including China, Taiwan, Sea of Japan, Indonesia, Thailand,
Russia, Hawaii, North American Pacific coast, North American
Atlantic and Gulf Coast, Caribbean, Central and South American
Pacific Coast, South American Atlantic coast, the Atlantic coast
in Europe, South Africa, Madagascar, the Red Sea, the Indian
Ocean, the Indo-Pacific, New Zealand, and Australia. Literature
searches produced only three species with planktotrophic
larvae that are currently grown for aquaculture [Strombus
pugilis (Linnaeus, 1758), Concholepas concholepas (Bruguiere,
1789), Babylonia areolata (Link, 1807)] and one species that is
under consideration for future aquaculture [Dicathais orbita
(Gmelin, 1791)].
Sixty-seven percent of the publications included in this
review (84) were studies of feeding larvae. This included a total
of 182 separate experiments with a total of 645 total treatments.
For experiments with feeding larvae, 90% (163) reported the
temperature, 98% (178) reported the food species that the
larvae were fed, 75% (137) reported the feeding frequency,
78% (142) reported the food concentration, 92% (167) reported
larval density, 30% (55) reported the time to competency in
larvae, and 32% (59) reported the time to metamorphosis.
Survivorship was reported in 51% (92) of experiments.
Temperature
Time to Metamorphosis
Of the 645 experimental treatments with planktotrophic
larvae, only 138 (21.4%) reported both temperature and time to
metamorphosis. For planktotrophic larvae, overall, there was
a significant negative correlation between temperature and time
to metamorphosis (n¼138, P¼0.0016, r¼0.266; Fig. 2).
With warmer temperature, larvae developed faster. This pat-
tern, however, was driven primarily by Crepidula fornicata,
which displayed a strong negative correlation between temper-
ature and time to metamorphosis (n¼47, P¼0.036, r¼0.307;
Fig. 2). There was no correlation between temperature and time
to metamorphosis for caenogastropods other than C. fornicata
or neogastropods (n¼48, P¼0.168), or for just the Neo-
gastropoda (n¼18, P¼0.937). There was, however, a positive
correlation between temperature and time to metamorphosis
for the Heterobranchia (n¼25, P¼0.025, r¼0.448; Fig. 2).
Figure 1. The number of studies on gastropod larvae by year included in this systematic review. The literature from 1840 to December 14, 2016, was
reviewed. The first article to fit the criteria of this review was published in 1967.
GASTROPOD LARVAL DEVELOPMENT 853
TABLE 1.
Species that were the focus of research included in this review.
Currently accepted
species name
Species name
as in publication
Developmental
mode Major clade
No. of
publications
No. of experimental
treatments
Crepidula fornicata C. fornicata Planktotrophic Caenogastropoda 33 281
Lobatus gigas Strombus gigas Planktotrophic Caenogastropoda 8 62
Ergaea walshi Crepidula plana Planktotrophic Caenogastropoda 5 40
Crepidula onyx C. onyx Planktotrophic Caenogastropoda 4 39
Strombus pugilis S. pugilis Planktotrophic Caenogastropoda 3 7
Laevistrombus canarium Strombus canarium Planktotrophic Caenogastropoda 2 21
Echinolittorina hawaiiensis Littorina picta Planktotrophic Caenogastropoda 1 28
Lobatus costatus Strombus costatus Planktotrophic Caenogastropoda 1 19
Ceraesignum maximum Dendropoma maximum Planktotrophic Caenogastropoda 1 5
Crepipatella lingulata Crepidula lingulata Planktotrophic Caenogastropoda 1 3
Crepipatella peruviana Crepipatella fecunda Planktotrophic Caenogastropoda 1 3
Cryptonatica janthostoma C. janthostoma Planktotrophic Caenogastropoda 1 1
Littorina littorea L. littorea Planktotrophic Caenogastropoda 1 1
Peringia ulvae Hydrobia ulvae Planktotrophic Caenogastropoda 1 1
Bittiolum alternatum Bittium alternatum Planktotrophic Caenogastropoda 1 1
Concholepas concholepas C. concholepas Planktotrophic Caenogastropoda Neogastropoda 4 13
Tritia obsoleta Ilyanassa obsoleta Planktotrophic Caenogastropoda Neogastropoda 4 12
Babylonia areolata B. areolata Planktotrophic Caenogastropoda Neogastropoda 2 4
Dicathais orbita D. orbita Planktotrophic Caenogastropoda Neogastropoda 1 21
Rapana venosa R. venosa Planktotrophic Caenogastropoda Neogastropoda 1 16
Babylonia formosae habei B. formosae habei Planktotrophic Caenogastropoda Neogastropoda 1 10
Conus flavidus C. flavidus Planktotrophic Caenogastropoda Neogastropoda 1 3
Conus marmoreus C. marmoreus Planktotrophic Caenogastropoda Neogastropoda 1 3
Conus striatus C. striatus Planktotrophic Caenogastropoda Neogastropoda 1 3
Conus lividus C. lividus Planktotrophic Caenogastropoda Neogastropoda 1 2
Conus pennaceus C. pennaceus Planktotrophic Caenogastropoda Neogastropoda 1 2
Conus quercinus C. quercinus Planktotrophic Caenogastropoda Neogastropoda 1 1
Kelletia kelletii K. kelletii Planktotrophic Caenogastropoda Neogastropoda 1 1
Onchidium reevesii Onchidium struma Planktotrophic Heterobranchia 2 4
Aplysia californica A. californica Planktotrophic Heterobranchia 1 27
Spurilla neapolitana S. neapolitana Planktotrophic Heterobranchia 1 3
Elysia viridis E. viridis Planktotrophic Heterobranchia 1 2
Philine aperta P. aperta Planktotrophic Heterobranchia 1 2
Amphibola crenata A. crenata Planktotrophic Heterobranchia 1 1
Hydatina physis H. physis Planktotrophic Heterobranchia 1 1
Palio dubia P. dubia Planktotrophic Heterobranchia 1 1
Babylonia formosae B. formosae Lecithotrophic Caenogastropoda Neogastropoda 1 4
Adalaria proxima A.proxima Lecithotrophic Heterobranchia 1 2
Lottia digitalis L. digitalis Lecithotrophic Patellogastropoda 1 2
Haliotis rufescens H. rufescens Lecithotrophic Vetigastropoda 12 60
Haliotis diversicolor H. diversicolor Lecithotrophic Vetigastropoda 5 30
Haliotis iris H. iris Lecithotrophic Vetigastropoda 5 15
Haliotis discus hannai H. discus hannai Lecithotrophic Vetigastropoda 3 4
Haliotis asinina H. asinina Lecithotrophic Vetigastropoda 2 12
Haliotis rubra H. rubra Lecithotrophic Vetigastropoda 2 12
Haliotis laevigata H. laevigata Lecithotrophic Vetigastropoda 2 9
Haliotis discus H. discus Lecithotrophic Vetigastropoda 2 6
Haliotis australis H. australis Lecithotrophic Vetigastropoda 1 26
Haliotis virginea H. virginea Lecithotrophic Vetigastropoda 1 15
Haliotis kamtschatkana H. kamtschatkana Lecithotrophic Vetigastropoda 1 1
Haliotis mariae H. mariae Lecithotrophic Vetigastropoda 1 1
Tectus pyramis T. pyramis Lecithotrophic Vetigastropoda 1 1
Alderia modesta A. modesta Poecilogony Heterobranchia 3 8
Tenellia adspersa T. adspersa Poecilogony Heterobranchia 1 4
Alderia willowi A. willowi Poecilogony Heterobranchia 1 2
Dendronotus frondosus D. frondosus Poecilogony Heterobranchia 1 2
Phestilla sibogae P. sibogae Poecilogony Heterobranchia 1 1
Species are sorted within each major clade by the number of publications and then the number of experimental treatments for that species.
PADILLA ET AL.854
Figure 2. Effect of temperature on life history metrics for planktotrophic larvae. Regression lines [ordinary least squares (OLS)] are displayed only
for groups with significant (P#0.05) correlations (— all data, — — Crepidula fornicata,‒‒Neogastropoda, — d— Caenogastropoda other than
C. fornicata or Neogastropoda, and ddd Heterobranchia). (A) Temperature and time to metamorphosis. Significant correlations for all planktotrophs
(Y$0.8642 +41.614, R
2
$0.0711), C. fornicata (Y$0.6556x+34.036, R
2
$0.0942), and Heterobranchia (Y$5.9578x94.724, R
2
$0.2011).
(B) Temperature and % survivorship. Significant correlations for C. fornicata (Y$4.3415x7.2052, R
2
$0.233) and Caenogastropoda other than
C. fornicata and Neogastropoda (Y$3.1308 +143.86, R
2
$0.0767). (C) Temperature and growth rate. Significant correlations for all
planktotrophs (Y$1.3745x3.5672, R
2
$0.032), C. fornicata (Y$5.124x75.149, R
2
$0.123), and Neogastropoda (Y$1.9137x25.282,
R
2
$0.1483).
GASTROPOD LARVAL DEVELOPMENT 855
Survivorship
There were data for survivorship and temperature for 314
(48.7%) experimental treatments with planktotrophic larvae.
There was no effect of temperature on survivorship for plank-
totrophic larvae overall (n¼314, P¼0.172), or for the
Neogastropoda (n¼45, P¼0.600) or Heterobranchia
(n¼28, P¼0.165). There was a positive correlation between
temperature and survivorship for Crepidula fornicata (n¼116,
P<0.0001, r¼0.483), the single most studied species with
planktotrophic larvae. There was, however, a negative correla-
tion between temperature and survivorship for the remaining
caenogastropods other than C. fornicata that were not neo-
gastropods (n¼127, P¼0.002, r¼0.277; Fig. 2).
Growth
There were data on growth and temperature for 273 (42.3%)
experimental treatments with planktotrophic larvae. Overall,
there was a significant positive effect of temperature on feeding
larval growth (n¼273, P<0.003, r¼0.179; Fig. 2). There was
no correlation between temperature and growth for the caeno-
gastropods that were not Crepidula fornicata or neogastropods
(n¼109, P¼0.216), but there was a positive correlation for
C. fornicata (n¼87, P¼0.0008, r¼0.351; Fig. 2) and for the
neogastropods (n¼50, P¼0.0057, r¼0.385; Fig. 2). All
experiments with heterobranchs were conducted at the same
temperature.
Larval Density
Time to Metamorphosis
Of the 645 experimental treatments with planktotrophic larvae,
only 140 (21.7%) reported both larval density and time to
metamorphosis. For planktotrophic larvae, overall, there was
a significant positive correlation between larval density and time
to metamorphosis (n¼140, P<0.0001, r¼0.354; Fig. 3). At
higher larval densities, time to metamorphosis was longer. This
pattern was driven primarily by species of Caenogastropoda
other than Crepidula fornicata that were not in the Neogastropoda
(n¼51, P¼0.0022, r¼0.420; Fig. 3) and the Heterobranchia
(n¼24, P¼0.0003, r¼0.707; Fig. 3). For Neogastropoda (n¼18,
P¼0.1027) and C. fornicata (n¼47, P¼0.825), there was no
correlation between larval density and time to metamorphosis.
Survivorship
There were data for survivorship and larval density for 311
(48.2%) experimental treatments with planktotrophic larvae.
There was no overall effect of larval density on survivorship
(n¼311, P¼0.065), or for just the Caenogastropoda (n¼283,
P¼0.982) or for Neogastropoda (n¼45, P¼0.354). There was
a negative correlation between larval density and survivorship
for Crepidula fornicata (n¼115, P<0.0001, r¼0.346; Fig. 3)
and a negative correlation between survivorship and larval
density for Heterobranchia (n¼28, P¼0.017, r¼0.448;
Fig. 3). There was a positive correlation between larval density
for species of caenogastropod other than C. fornicata that were
not neogastropods (n¼123, P¼0.008, r¼0.241; Fig. 3).
Growth
There were data on both larval density and growth for 283
(43.9%) experimental treatments with planktotrophic larvae.
Overall, there was no effect of larval density on growth
(n¼283, P¼0.075), or for all caenogastropods (n¼256, P¼
0.383; Fig. 3); however, there was a significant positive correla-
tion for Neogastropoda (n¼49, P¼0.0023, r¼0.427; Fig. 3)
and a significant negative correlation between larval density and
growth for Crepidula fornicata (n¼99, P¼0.028, r¼0.221;
Fig. 3). There was also no correlation between larval density and
growth for the Heterobranchia (n¼27, P¼0.661).
Food Density
Time to Metamorphosis
Of the 645 experimental treatments with planktotrophic
larvae, only 127 (19.7%) reported both food density and time to
metamorphosis. For planktotrophic larvae, overall, there was
a significant positive correlation between food density and time
to metamorphosis (n¼127, P<0.001, r¼0.321; Fig. 4). This
pattern, however, was driven by differences among taxa. There
was no significant correlation for all caenogastropods together
(n¼103, P¼0.576), or caenogastropods other than Crepidula
fornicata or the neogastropods (n¼46, P¼0.933). For
neogastropods (n¼10, P¼0.069) and heterobranchs
(n¼24, P¼0.238), there was also no significant correlation
between food density and time to metamorphosis. For
C. fornicata, all experiments that reported both food density
and time to metamorphosis (n¼47) were conducted with the
same food density (1.8 310
5
cells/mL). At this food density,
reported time to metamorphosis ranged from 11 to 36 days.
Survivorship
There were data for survivorship and planktonic food
density for 290 (44.9%) experimental treatments with plankto-
trophic larvae. There was no overall effect of food density on
survivorship (n¼290, P¼0.381). There was no correlation
between food density and survivorship for all of the Caenogas-
tropoda (n¼262, P¼0.330), for just the Neogastropoda
(n¼28, P¼0.350), or for Crepidula fornicata (n¼115,
P¼0.689). Similarly, there was no correlation for the Hetero-
branchia (n¼28, P¼0.459).
Growth
There were data on food density and growth for 248
(38.6%) experimental treatments with planktotrophic larvae.
Overall, there was no significant effect of food density on
growth (n¼248, P¼0.932). This pattern was consistent for all
caenogastropods (n¼221, P¼0.752) and caenogastropods
other than Crepidula fornicata that were not neogastropods
(n¼106, P¼0.891). For C. fornicata (n¼87, P<0.001,
r¼0.522; Fig. 4) and neogastropods (n¼28, P¼0.001,
r¼0.611; Fig. 4), however, there was a significant positive
correlation between food density and larval growth. There was
no correlation for the heterobranchs (n¼27, P¼0.870).
Per Capita Food Availability
Time to Metamorphosis
Of the 645 experimental treatments with planktotrophic
larvae, only 111 (17.2%) reported per capita food availability
(food concentration and larval concentration) and time to
metamorphosis. For planktotrophic larvae, overall, there was
PADILLA ET AL.856
Figure 3. Effects of larval density on life history metrics for planktotrophic larvae. Ordinary least squares regression lines are displayed only for groups
with significant (P#0.05) correlations (— all data, — — Crepidula fornicata,‒‒Neogastropoda, — d— Caenogastropoda other than C. fornicata or
Neogastropoda, and ddd Heterobranchia). (A) Larval density and time to metamorphosis. Significant correlations for all planktotrophs (Y$2.7891x+
19.759, R
2
$0.1245), Caenogastropoda that are neither C. fornicata nor neogastropods (Y$1.9633x+14.744, R
2
$0.1758), and Heterobranchia
(Y$5.1343x+28.85, R
2
$0.4495). (B) Larval density and % survivorship. Significant correlations for C. fornicata (Y$14.655x+92.64, R
2
$0.1198),
Caenogastropoda other than C. fornicata or Neogastropoda (Y$24.531x+53.818, R
2
$0.0577), and Heterobranchia (Y$14.407 +71.654,
R
2
$0.20 06). (C ) Larval density and growth rate. Significant correlations for C. fornicata (Y$35.021x+48.806, R
2
$0.0486) and Neogastropoda
(Y$16.721x+15.263, R
2
$0.1815).
GASTROPOD LARVAL DEVELOPMENT 857
no significant correlation between per capita food availability
and time to metamorphosis (n¼111, P¼0.538). Within taxa,
there was also no correlation except for the heterobranchs,
which showed a negative correlation (n¼24, P¼0.002,
r¼0.609; Fig. 5). Removal of the outlier data point did not
change the significance of this correlation (n¼23, P¼0.004,
r¼0.573). There was no correlation for all caenogastropods
together (n¼87, P¼0.566), for caenogastropods other than
Crepidula fornicata that were not neogastropods (n¼31,
P¼0.856), or for C. fornicata (n¼47, P¼0.410). All
experiments with Neogastropoda (n¼9) were conducted with
the same per capita food availability.
Survivorship
Thereweredataforsurvivorship and per capita food
availability for 259 (40.2%) experimental treatments with
planktotrophic larvae. There was no overall effect of per
capita food density on survivorship (n¼259, P¼0.653).
But, there was a significant positive correlation for the
Heterobranchia (n¼28, P¼0.028, r¼0.415; Fig. 5). There
was no correlation between per capita food density and
survivorship for the Caenogastropoda overall (n¼231,
P¼0.798) or the Caenogastropoda other than Crepidula
fornicata that were not neogastropods (n¼102, P¼0.205).
There was a significant positive correlation between per capita
food availability and survivorship for the neogastropods (n¼18,
P<0.0001, r¼0.887). Survivorship increased with increased per
capita food availability. For C. fornicata, there was a significant
negative correlation between per capita food availability and
survivorship (n¼111, P¼0.033, r¼0.202); higher per capita
food availability was associated with lower survivorship.
Growth
There were data on per capita food availability and growth for
242 (37.3%) experimental treatments with planktotrophic larvae.
Overall, there was a significant positive effect of per capita food
density on growth (n¼242, P¼0.001, r¼0.202; Fig. 5). This
pattern was consistent for all of the caenogastropods together
(n¼215, P¼0.006, r¼0.187; Fig. 5), for caenogastropods other
than Crepidula fornicata that were not neogastropods (n¼106,
P¼0.026, r¼0.217; Fig. 5), for just C. fornicata (n¼82,
P¼0.005, r¼0.374; Fig. 5), and for just the neogastropods (n¼
27, P¼0.002, r¼0.560; Fig. 5). There was no correlation,
however, for the heterobranchs (n¼27, P¼0.128).
Lecithotrophic Larvae
For species with lecithotrophic larvae, there were 46
articles, 81 experiments, and a total of 216 experimental
treatments for 27 currently recognized species or subspecies
of gastropods from only five genera (Table 1). This included
one species of Patellogastropoda, 13 species of Vetigastro-
poda, 12 of which are in the genus Haliotis, one species of
Caenogastropoda that is also in the Neogastropoda, and one
species in the Heterobranchia. The vast majority of the
gastropods studied were herbivores, and only one was a predator
and one was a scavenger.
Of the species with lecithotrophic larvae that were found in
the literature search, only two live in the intertidal zone; the rest
were species found in the subtidal zone. As for the gastropod
species with planktotrophic larvae, studied species were from
a wide range of geographic areas including China, Sea of Japan,
Indonesia, Russia, North American Pacific coast, North American
Atlantic, South American Pacific Coast, Atlantic coast in Europe,
North Africa, Mediterranean, Arabian Sea, the Indian Ocean, the
Indo-Pacific, New Zealand, and Australia. Nine of the recognized
species and subspecies with lecithotrophic larvae are grown in
aquaculture.
Lecithotrophic larvae were the focus of 37% (46) of all of the
publications in the review. For lecithotrophic larvae, there were
81 different experiments and 216 total different treatment levels.
Temperature was reported in 80% treatments that focused on
lecithotrophic larvae and 44% reported time to metamorphosis.
Temperature
Time to Metamorphosis
Of the 216 experimental treatments with lecithotrophic
larvae, only 76 (35%) reported both temperature and time
to metamorphosis. For nonfeeding larvae, overall, there was
no significant correlation between temperature and time to
metamorphosis (n¼76, P¼0.654). There was a significant positive
correlation, however, for the Heterobranchia (n¼9, P¼0.012,
r¼0.786; Fig. 6). This correlation was primarily driven by a single
outlying point; removal of that one data point resulted in no
Figure 4. Effects of food concentration on life history metrics for plankto-
trophic larvae. Ordinary least squaresregression lines are displayed only for
groups with significant (P#0.05) correlations (— all data, — — Crepidula
fornicata,and‒‒Neogastropoda). (A) Food concentration and time to
metamorphosis. Significant correlation for all planktotrophs (Y$23
10
5
x+17.917, R
2
$0.1034). (B) Food concentration and growth rate.
Significant correlations for C. fornicata (Y$0.0003x+1.8521, R
2
$0.2728)
and Neogastropoda (Y$0.0002x+8.3205, R
2
$0.3737).
PADILLA ET AL.858
correlation (n¼8, P¼0.259). These data were from only three
publications (Miller & Hadfield 1986, Chester 1996, Sisson 2002),
and eight of the experimental treatments were for two closely
related species, Tenellia adspersa and Phestilla sibogae.Therewas
a significant negative correlation for the Vetigastropoda (n¼61,
P¼0.0106, r¼0.325); vetigastropods developed slower at higher
temperatures. The abalone Haliotis rufescens was the most studied
species with nonfeeding larvae. There were only five experimental
treatments (from four publications) where both temperature and
time to metamorphosis were reported. For the available data, there
was no significant relationship (n¼5, P¼0.460).
Survivorship
There were data for survivorship and temperature for
72 (33.3%) experimental treatments with nonfeeding larvae.
For neogastropods, all six experimental treatments were conduct-
ed at the same temperature and had the same survivorship. But,
there was a significant negative correlation between temperature
and survivorship for lecithotrophic larvae overall (n¼72,
P¼0.002, r¼0.356; Fig. 6). Similarly, there was a significant
negative correlation between temperature and survivorship for
heterobranchs (n¼6, P¼0.004, r¼0.950; Fig. 6), as well as for
the vetigastropods (n¼60, P¼0.005, r¼0.354; Fig. 6). For
Haliotis rufescens (n¼26, P<0.0001, r¼0.830), the single most
studied species of lecithotroph, again there was a negative
correlation between temperature and survivorship. The data
for this species seem to indicate a temperature threshold, below
which survivorship drops (Fig. 6). There were too few data to
determine if other species show a similar threshold pattern.
Growth
There were data on growth and temperature for only nine
experimental treatments for nonfeeding larvae, and all studies
were on vetigastropods. There was no significant effect of temper-
ature on larval growth for this group (n¼9, P¼0.178).
Larval Density
Time to Metamorphosis
Of the 216 experimental treatments with nonfeeding larvae,
only 66 (30.5%) reported both larval density and time to
Figure 5. Effect of food per capita on life history metrics for planktotrophic larvae. Ordinary least squares regression lines are displayed only for groups
with significant (P#0.05) correlations (all data, — — Crepidula fornicata,‒‒Neogastropoda, — d— Caenogastropoda other than C. fornicata or
Neogastropoda, and ddd Heterobranchia). (A) Food per capita and growth rate. Significant correlations for all planktotrophs (Y$9310
7
x+28.894, R
2
$0.0414), C. fornicata (Y$4310
6
x+37.629, R
2
$0.1399), Neogastropods (Y$7310
5
x+9.169, R
2
$0.3136), and Caenogastropoda other than
C. fornicata or Neogastropoda (Y$5310
7
+26.972, R
2
$0.0467). (B) Food per capita and time to metamorphosis. Significant correlation for
Heterobranchia (Y$2310
5
x+40.786, R
2
$0.371). (C) Food per capita and % survivorship for C. fornicata alone (Y$2310
6
x+86.808, R
2
$
0.041). (D) Food per capita and % survivorship for all taxonomic groups except C. fornicata. Significant correlations for Neogastropoda (Y$0.0003x+
2.7539, R
2
$0.7866) and Heterobranchia (Y$4310
5
x+40.308, R
2
$0.1719).
GASTROPOD LARVAL DEVELOPMENT 859
metamorphosis. For nonfeeding larvae, overall, there was no
correlation between larval density and time to metamorphosis
(n¼66, P¼0.3953). Similarly, there were no correlations
between larval density and time to metamorphosis for neogastropods
(n¼6, P¼0.1849) or for vetigastropods (n¼56, P¼0.1003),
including Haliotis rufescens (n¼4, P¼0.7178). All hetero-
branchs that were studied (n¼4) had a larval density of
2 larvae/mL and metamorphosed in 10 days.
Survivorship
There were data for survivorship and larval density for 51
(23.6%) experimental treatments with lecithotrophic larvae.
Overall, there was a positive correlation between larval density
and survivorship (n¼51, P¼0.017, r¼0.332; Fig. 6). This
relationship was driven by two outlying points; removal of
those two data points resulted in no significant correlation
(n¼49, P¼0.096). There was a positive correlation between
larval density and survivorship for neogastropods (n¼6,
P¼0.023, r¼0.851; Fig. 6) and for vetigastropods (n¼43,
P¼0.0017, r¼0.465; Fig. 6). For just Haliotis rufescens, there
was a significant positive correlation (n¼11, P¼0.002,
r¼0.818). There were data for only two experimental treat-
ments with heterobranchs; therefore, it was not possible to test
for a correlation for this clade.
Growth
There were data on larval density and growth for nine
(4.2%) experimental treatments with lecithotrophic larvae. All
nine of these experimental treatments came from two studies
(Pena 1985, Stott et al. 2004) and were for the same genus,
Haliotis (Haliotis diversicolor aquatilis and Haliotis discus).
Overall, there was a marginally significant positive effect of
larval density on growth (n¼9, P¼0.052, r¼0.662), but this
was driven by one outlier. When this point was removed, there
was no significant relationship (n¼8, P¼0.812).
DISCUSSION
Gastropod larvae have been studied in the laboratory for
decades, with most publications on rearing larvae under
experimental conditions through metamorphosis appearing
since the mid—1960s (Fig. 1). Considerable information is
available for certain species, particularly commercially impor-
tant species, such as abalone (Haliotis spp.), as well as one
species of slipper shell Crepidula fornicata. Although hundreds
of studies have been published, surprisingly few report impor-
tant metadata that allow general questions to be addressed. In
addition, most studies have been carried out on relatively few
species. This limits the ability to generalize across taxa.
All Patellogastropoda and Vetigastropoda have lecithotro-
phic larvae. Within the Caenogastropoda and Heterobranchia,
there is a mixture of developmental types, but among those
species studied, the vast majority are planktotrophs. To tell
whether there are clade-specific patterns among taxa with
planktotrophic development, more studies are needed on
different species with planktotrophic development. Generally,
species with lecithotrophic larvae are underrepresented in the
literature, and more work is needed on species across clades
with this developmental mode. Too few species with poecilog-
ony were studied to determine if there were patterns associated
with that mode of development.
Although many different factors could be confounded with,
or contribute to, the patterns of time to metamorphosis,
survivorship, and larval growth that were examined, some
patterns within and across clades and modes of development
Figure 6. Factors affecting life history metrics of lecithotrophic larvae. Ordinary
least squares regression lines are displayed only for groups with significant (P#
0.05) correlations (— all data, dd Vetigastropoda, ‒‒Neogastropoda, and
dddHeterobranchia). (A) Temperature and time to metamorphosis. Significant
correlations for the Vetigastropoda (Y$0.1783x+7.4177, R
2
$0.1057) and
the Heterobranchia (Y$0.4407x1.2435, R
2
$0.6174). (B) Temperature
and % survivorship. Significant correlations for all lecithotrophs (Y$1.8673x+
98.179, R
2
$0.1265), Vetigastropoda (Y$1.9007x+98.234, R
2
$0.1255),
and Heterobranchia (Y$4.0524x+121.93, R
2
$0.9016). (C) Larval density
and % survivorship. Significant correlations for all lecithotrophs (Y$1.0753x+
40.288, R
2
$0.1105), Vetigastropoda (Y$1.4588x+29.511, R
2
$0.2163), and
Neogastropoda (Y$5.4172x+59.642, R
2
$0.7246).
PADILLA ET AL.860
did emerge. In all cases, there was considerable variance in the
data, which is reflected in the relatively low correlations
observed.
Temperature
For species with planktotrophic larvae, in general, increased
temperature tended to decrease development time as measured
by time to metamorphosis, except for the heterobranchs. There
were conflicting patterns for the effects of temperature on larval
survivorship. Across all planktotrophs, and for just the neo-
gastropods and the heterobranchs, there was no correlation
between temperature and survivorship. Warmer temperatures,
however, were correlated with increased survivorship for Crep-
idula fornicata and decreased survivorship for the remaining
caenogastropods. In general, increased temperature was corre-
lated with increased growth except for caenogastropods other
than C. fornicata or neogastropods (Table 2).
For gastropods with lecithotrophic larvae, increased tem-
perature was correlated with shorter time to metamorphosis
for vetigastropods, but the opposite was true for the hetero-
branchs. The sample size for heterobranchs, however, was
quite small (n¼9). Across all taxa with lecithotrophic larvae,
there was no pattern for effects of temperature on time to
metamorphosis (Table 3).
For gastropods with lecithotrophic development, and all
clades with sufficient sample sizes to test for correlations,
increased temperature was correlated with decreased survivor-
ship and had no effect on growth, but data on growth were very
limited (Table 3).
Increased temperature is generally associated with increased
metabolic rate and faster development (Clarke 2006, Pappa-
lardo et al. 2014, Watson et al. 2014), which was seen in some,
but not all, groups of both planktotrophic and lecithotrophic
gastropod larvae. For gastropods with lecithotrophic larvae,
including all clades that could be tested, increased temperature
was associated with decreased survivorship, suggesting that
there may be an energetic cost to more rapid development or to
dealing with physiological stress of increased temperature. For
most groups of gastropods with planktotrophic larvae, survi-
vorship was not correlated with temperature. Exceptions were
the caenogastropods other than Crepidula fornicata and neo-
gastropods, which showed a similar trend as that seen for
lecithotrophs. For C. fornicata, increased temperature was
actually correlated with higher survivorship. The counter trend
for C. fornicata is curious. Studies with this species fell within
a narrower temperature range than those for other taxa.
Clearly, more data are needed to test the effects of temperature
on survivorship of C. fornicata over a wider range of temper-
ature and for more taxa. In addition, data on the metabolic and
physiological costs of temperature-dependent development
rates, temperature stress, and the energetics of metabolic de-
mand are needed.
Larval Density
Larval density can affect food competition for feeding
larvae, as well as interference among larvae, reducing individual
feeding time or efficiency. Overall, there were few, and some-
times conflicting, patterns for the association between larval
density for gastropod species with planktotrophic development
and the response metrics examined in this review. When all data
for planktotrophic larvae were considered together, increased
density was associated with an increase in the time to meta-
morphosis. This trend was, however, only apparent when all
species were considered together. No significant pattern was
found for species of caenogastropods other than Crepidula
fornicata that were not neogastropods or for the heterobranchs.
There was no relationship between larval density and develop-
ment time for the neogastropods or for C. fornicata (Table 2).
Although time to metamorphosis was not correlated with larval
density for C. fornicata, increased larval density was correlated
TABLE 2.
Summary of correlations among factors examined for planktotrophic larvae.
Caenogastropoda
Heterobranchia
All
planktotrophsAll
Non-Neogastropoda,
non-Crepidula fornicata
Just
C. fornicata
Just
Neogastropoda
Temperature
Time to metamorphosis Yn¼113, 18.4% ;n¼48, 19.8% Yn¼47, 16.7% ;n¼18, 20.2% [n¼25, 78.1% Yn¼138, 21.4%
Survivorship ;n¼286, 46.7% Yn¼130, 53.5% [n¼116, 41.3% ;n¼45, 50.6% ;n¼28, 87.5% ;n¼314, 48.7%
Growth [n¼246, 40.1% ;n¼109, 44.9% [n¼87, 31.0% [n¼50, 56.2% [n¼273, 42.3%
Larval density
Time to metamorphosis [n¼116, 18.9% [n¼51, 21.0% ;n¼47, 16.7% ;n¼18, 20.2% [n¼24, 75.0% [n¼140, 21.7%
Survivorship ;n¼283, 46.2% [n¼123, 50.6% Yn¼115, 40.9% ;n¼45, 50.6% Yn¼28, 87.5% ;n¼311, 48.2%
Growth ;n¼256, 41.8% ;n¼108, 44.4% Yn¼99, 35.2% [n¼49, 55.1% ;n¼27, 84.4% ;n¼283, 43.9%
Food density
Time to metamorphosis ;n¼103, 16.8% ;n¼46, 18.9% ;n¼10, 11.2% ;n¼24, 75.0% [n¼127, 19.7%
Survivorship ;n¼262, 42.7% ;n¼119, 49.0% ;n¼115, 40.9% ;n¼28, 31.5% ;n¼28, 87.5% ;n¼290, 45.0%
Growth ;n¼221, 36.1% ;n¼106, 43.6% [n¼87, 31.0% [n¼28, 31.5% ;n¼27, 84.4% ;n¼248, 38.6%
Per capita food availability
Time to metamorphosis ;n¼87, 14.2% ;n¼31, 12.8% ;n¼47, 16.7% Yn¼24, 75.0% ;n¼111, 17.2%
Survivorship ;n¼231, 37.7% ;n¼102, 42.0% Yn¼111, 39.5% [n¼18, 20.2% [n¼28, 87.5% ;n¼259, 40.2%
Growth [n¼215, 35.1% [n¼106, 43.6% [n¼82, 29.2% [n¼27, 30.3% ;n¼27, 84.4% [n¼242, 37.3%
[indicates a significant positive correlation, Yindicates a significant negative correlation, and ;indicates no significant correlation. – indicates
calculation of a correlation was not possible. n¼sample size and the percent of the total number of experimental treatments for each clade.
GASTROPOD LARVAL DEVELOPMENT 861
with reduced survivorship. Increased larval density was also
correlated with reduced survivorship for the heterobranchs;
however, there was no overall trend in the effect of larval density
on survivorship among planktotrophic species, or for the
caenogastropods overall or the neogastropods. Surprisingly,
increased larval density was correlated with higher survivorship
for species of caenogastropods other than C. fornicata and
neogastropods (Table 2), as was seen for species with lecitho-
trophic larvae (Table 3).
Overall, for species with planktotrophic larvae, there was no
significant relationship between larval density and larval growth.
There was also no relationship for the clades Heterobranchia or
Caenogastropoda overall. Increased larval density was corre-
lated with slower growth for Crepidula fornicata, but it was
correlated with faster growth for neogastropods (Table 2). The
lack of consistent patterns among clades may mean that density
per se is relatively less important, and what is more important is
how density affects other factors such as food availability (see
per capita food availability). More data across taxa are
needed before strong conclusions can be drawn.
For lecithotrophic larvae, there was no significant relationship
between larval density and development time overall or among clades
with enough data to test for a correlation (Table 3). For the studies
included in this review, however, increased larval density was
correlated with increased survivorship overall, as well as for just
neogastropods and for just vetigastropods. Similarly, there was
a positive relationship between larval density and growth rate, but
this pattern was for only nine experimental treatments with vetigas-
tropods; no other taxa were examined (Table 3). Positive correla-
tions between larval density and survivorship or growth are
curious and need further experiments across more taxa to
determine if these relationships are robust. In addition, possible
mechanisms that could produce this pattern are needed.
Food Density
Overall, increased food density was positively correlated with
increased time to metamorphosis for all species with planktotrophic
development; however, this pattern was driven by differences
among clades. There was no relationship between food density
and development time for any clade (Table 2). All studies that
reported food density and time to metamorphosis for Crepidula
fornicata were conducted at the same food density. Interestingly,
when provided with the same food density, larval metamorphosis
ranged more than 3-fold, from 11 to 36 days. Thus, it appears that
for this species, overall food density alone is not a major factor
controlling development time. There was no relationship between
food density and survivorship for planktotrophic larvae overall, or
for any clade tested (Table 2). Increased food density was
correlated with increased growth for neogastropods and for
C. fornicata, but there was no similar correlation for other taxa
or overall (Table 2).
Per Capita Food Availability
Per capita food availability combines the effects of larval density
and food concentration. Interestingly, there was no relationship
between per capita food availability and time to metamorphosis for
planktotrophic larvae overall, for the caenogastropods overall, or
for any group within the caenogastropods examined. There was
a negative correlation between per capita food availability and time
to metamorphosis for the heterobranchs, indicating that higher per
capita food resulted in faster development. This result suggests that
food competition among larvae is important for development time
as this group showed no correlation between food density and time
to metamorphosis and a positive correlation between larval density
and time to metamorphosis (Table 2). Per capita food availability
was correlated with higher survivorship for neogastropods and
heterobranchs but was surprisingly correlated with reduced survi-
vorship for Crepidula fornicata. This difference could be affected by
differences among studies in the method used to determine survivor-
ship. Further experimentation and documentation of methods are
needed to determine if this pattern is robust. Overall, there was no
correlation between per capita food availability and survivorship for
planktotrophs. On the other hand, overall and for all of the different
taxa considered, except the heterobranchs, which showed no
pattern, faster larval growth was correlated with increased per
capita food availability (Table 2). Again, this suggests that food
competition among larvae may be most important. More experi-
ments are needed that test these patterns directly across species, as
well as with C. fornicata, as are studies designed to determine
mechanisms that may be responsible for these patterns.
Recommendations for Future Work
Drawing strong inference from a review such as the one
presented here has many limitations. In general, the ability to
TABLE 3.
Summary of correlations among factors examined for lecithotrophic larvae.
Neogastropoda Heterobranchia Vetigastropoda Patellogastropoda
All
Lecithotrophs
Temperature
Time to metamorphosis [n¼9, 56.3% Yn¼61, 31.8% ;n¼76, 35%
Survivorship Yn¼6, 37.5% Yn¼60, 31.3% Yn¼72, 33.3%
Growth ;n¼9, 4.7% ;n¼9, 4.2%
Larval density
Time to metamorphosis ;n¼6, 100% ;n¼56, 29.2% ;n¼66, 30.5%
Survivorship [n¼6, 100% [n¼43, 22.4% [n¼51, 23.6%
Growth [*n¼9, 4.7% [*n¼9, 4.2%
[indicates a significant positive correlation, Yindicates a significant negative correlation, ;indicates no significant correlation, and *indicates
correlation was marginally significant. – indicates calculation of a correlation was not possible. n¼sample size and the percent of the total number
of experimental treatments for each clade.
PADILLA ET AL.862
draw robust conclusions will always depend on the complete-
ness of the data used to draw inference. Although the Gastro-
poda is the largest class of the Mollusca with more than 62,000
species, surprisingly few species (57) have been studied with
experiments that follow the larval stage through metamorpho-
sis. For this review, most species were represented by only
a single publication, and many more species with planktotro-
phic development than those with lecithotrophic development
have been studied. The analyses presented could not take into
account the lack of independence created when different
numbers of species, or species within a genus, are represented
by a different number of studies, or the potential lack of
independence due to the same set of investigators producing
multiple studies, or the same geographic locations where studies
were conducted. The one species that has been studied most
extensively is the slipper snail Crepidula fornicata,which
represents more than 26% of all publications considered in this
review. It is clear, however, that it is not possible to attribute the
findings for this species to all gastropods with planktotrophic
development or even all caenogastropods with planktotrophic
development. For only two cases, the relationship between
warmer temperatures andfaster growth rates, and the correlation
between higher per capita food availability and faster larval
growth, was there a consistent response across taxa that were also
generally consistent with the response of C. fornicata. For the
species with lecithotrophic larvae included in this review, overall
patterns were generally more consistent across clades. Although
there are many species of caenogastropod with lecithotrophic
development, only a single species, Babylonia formosae (G. B.
Sowerby II, 1866), was included in this review, precluding us from
testing patterns for this clade. Most of the lecithotrophic species
with enough data to include in this review were vetigastropods,
primarily in the genus Haliotis (37 of 48 studies). Again, it is hard
to draw general conclusions when so few species have been studied
and when most studies are of closely related species.
Another challenge in finding generalizations among taxa is
that most studies do not report all of the metadata needed to
make comparisons among studies. To compare studies in the
future, it is important that certain metadata always be included.
Based on this review, recommendations would include always
reporting the temperature at which experiments were run and the
density of larvae in each experiment. For feeding larvae, it is also
important to report actual food concentration (e.g., not ad
libitum) and feeding frequency. Per capita food availability had
an important impact on growth performance and, in some cases,
survivorship of feeding larvae. Most studies (17%–40% among
clades) did not provide the information needed to calculate per
capita food availability. By examining the effects of per capita
food availability, the combined effects of food density and larval
density could be assessed. With more data for more species, it
would be feasible to examine the effects of multiple, potentially
interacting factors. For example, with the data set assessed for
this study, it was not possible to test combined effects of factors
such as temperature and food concentration, or temperature and
larval density on development time. The interplay of multiple
factors may be responsible for some of the counterintuitive
patterns detected in this study.
Equally important to the metadata are the response variables
that are reported, and information on how those response
variables were quantified. This review attempted to examine
time to metamorphosis, as a general indicator of developmental
rate, survivorship, and larval growth. Although not all studies
have the same goals, in many cases, some of these data were
collected during the course of an experiment but not reported in
publications. In addition, not every study uses the same metrics
to determine these response variables. For example, for time to
metamorphosis, some articles report the date of first individual to
metamorphose, whereas others report when 50%, 90%, or 100%
metamorphose. Whatever the case, where information is avail-
able, it would be most valuable if it is all reported. For survivor-
ship, it was found that different studies calculated survivorship
differently. In some cases, missing individuals were counted as
mortality, whereas in other cases, missing individuals were not
counted as mortality. In the latter case, if only 80% of individuals
were recovered and no dead larvae were found, it would be
reported as 100% survivorship. Again, to get around this
problem, simply reporting all data would be most useful, and
providing details of how metrics such as survivorship are de-
termined is essential. Reports of growth are typically more
uniform across studies, where the change in size over a certain
number of days is reported, and typically the age of the larvae is
provided. Although reporting all of these performance metrics
can be time consuming (particularly measuring growth or
extending an experiment until most animals metamorphose),
the ability to determine if there are general patterns among
species with particular developmental modes, or among major
taxa or species will increase with the availability of more data on
different species.
Ultimately, the abilityto examine all of the patterns discussed
in this review in a phylogenetic context is needed. This will
require good phylogenies at the species level within and across
clades. When such phylogenies are available, comparative
methods can be used to address questions about the evolution
of developmental mode or life history traits, and the impacts of
factors such as food abundance, temperature, and larval density.
ACKNOWLEDGMENTS
This work was funded in part by NSF grant IOS-0920032
(D. K. P.) and NSF DBI-1611997 (M. R.). This is contribution
number 1252 of the Department of Ecology and Evolution,
Stony Brook University.
LITERATURE CITED
Chester, C. M. 1996. The effect of adult nutrition on the reproduction
and development of the estuarine nudibranch, Tenellia adspersa
(Nordmann, 1845). J. Exp. Mar. Biol. Ecol. 198:113–130.
Clarke, A. 2006. Temperature and the metabolic theory of ecology.
Funct. Ecol. 20:405–412.
Krug, P. J., D. Gordon & M. R. Romero. 2012. Seasonal polyphenism
in larval type: rearing environment influences the development mode
expressed by adults in the sea slug Alderia willowi.Integr. Comp.
Biol. 52:161–172.
Miller, S. E. & M. G. Hadfield. 1986. Ontogeny of phototaxis and meta-
morphic competence in larvae of the nudibranch Phestilla sibogae Bergh
(Gastropoda: Opisthobranchia). J. Exp. Mar. Biol. Ecol. 97:95–112.
Padilla,D.K.,M.J.McCann,M.McCartyGlenn,A.P.Hooks&
S. E. Shumway. 2014. Effect of food on metamorphic
GASTROPOD LARVAL DEVELOPMENT 863
competence in the model system Crepidula fornicata.Biol. Bull.
227:242–251.
Pappalardo, P., E. Rodrıguez-Serrano & M. Fernandez. 2014. Corre-
lated evolution between mode of larval development and habitat in
muricid gastropods. PLoS One 9:e94104.
Pena, J. B. 1985. The culture of Haliotis discus Reeve (Gastropoda;
Prosobranchia) from fertilization to one-year-old in laboratory
conditions. Iberus 5:21–30.
Perron, F. E. 1981. Larval growth and metamorphosis of Conus
(Gastropoda: Toxoglossa) in Hawaii. Pac. Sci. 35:25–38.
Pullin, A. S. & G. B. Stewart. 2006. Guidelines for systematic review in
conservation and environmental management. Conserv. Biol.
20:1647–1656.
Seelemann, U. 1967. Rearing experiments on the amphibian slug
Alderia modesta.Helgoland. Wiss. Meer. 15:128–134.
Sisson, C. D. 2002. Dichotomous life history patterns for the nudi-
branch Dendronotus frondosus (Ascanius, 1774) in the Gulf of
Maine. Veliger 45:290–298.
Stott, A. E., T. Takeuchi & Y. Koike. 2004. An alternative culture
system for the hatchery production of abalone without using live-
food. Aquaculture 236:341–360.
Watson, S.-A., S. A. Morley, A. E. Bates, M. S. Clark, R. W. Day,
M. Lamare, S. M. Martin, P. C. Southgate, K. S. Tan, P. A. Tyler &
L. S. Peck. 2014. Low global sensitivity of metabolic rate to temper-
ature in calcified marine invertebrates. Oecologia 174:45–54.
LITERATURE USED IN THIS REVIEW
Affan, M. A.,H. S. Khomayis, J. Lee, S. M. Al-Harbi, H.E. Touliabah &
N. I. Abdulwassi. 2015. Settlement and growth of larval and
juvenile abalone on single and mixed strains of benthic diatoms.
Thalassas 31:59–65.
Aranda, D. A., A. Lucas, T. Brule, E. Salguero & F. Rendon. 1989.
Effects of temperature, algal food, feeding rate and density on the
larval growth of the milk conch (Strombus costatus) in Mexico.
Aquaculture 76:361–371.
Balkhair, M. A., A. R. Al-Mushikhi & M. V. Chesalin. 2013. Exper-
imental grow-out of the Omani abalone Haliotis mariae Wood,
1828, in land-based tanks in Mirbat, Oman. J. Shellfish Res. 32:37–
44.
Barile, P. J., A. W. Stoner & C. M. Young. 1994. Phototaxis and vertical
migration of queen conch (Strombus gigas Linne) veliger larvae.
J. Exp. Mar. Biol. Ecol. 183:147–162.
Blanchard, M., J. A. Pechenik, E. Giudicelli, J. Connan & R. Robert.
2008. Competition for food in the larvae of two marine molluscs,
Crepidula fornicata and Crassostera gigas.Aquat. Living Resour.
21:197–205.
Bohn, K., C. A. Richardson & S. R. Jenkins. 2013. Larval microhabitat
associations of the non-native gastropod Crepidula fornicata and
effects on recruitment success in the intertidal zone. J. Exp. Mar.
Biol. Ecol. 448:289–297.
Boxshall, A. J. 1999. The importance of flow and settlement cues to
larvae of the abalone, Haliotis rufescens Swainson. J. Exp. Mar.
Biol. Ecol. 254:143–167.
Brante, A., M. Fern
andez & F. Viard. 2008. Effect of oxygen conditions
on intracapsular development in two calyptraeid species with
different modes of larval development. Mar. Ecol. Prog. Ser.
368:197–207.
Brito-Manzano, N. & D. A. Aranda. 2002. Larval development model
of Strombus gigas versus Strombus pugilis.Proc. Gulf Caribb. Fish.
Inst. 53:266–275.
Brito-Manzano, N. & D. A. Aranda. 2004. Development, growth and
survival of the larvae of queen conch Strombus gigas under
laboratory conditions. Aquaculture 242:479–487.
Brito-Manzano, N. & D. A. Arada. 2013. Effect of photoperiod and
feeding schedule on growth and survival of larvae of the fighting
conch Strombus pugilis Linn
e, 1758 (Mollusca, Gastropoda). Aqua-
culture 408–409:47–50.
Cahill, A. E. & S. A. Koury. 2016. Larval settlement and metamorpho-
sis in a marine gastropod in response to multiple conspecific cues.
PeerJ 4:e2295.
Cam, S. L., J. A. Pechenik, M. Cagnon & F. Viard. 2009. Fast versus
slow larval growth in an invasive marine mollusc: does paternity
matter? J. Hered. 100:455–464.
Campos, E. O., A. Pinto, E. Bustos, S. R. Rodriguez & N. C. Inestrosa.
1994. Metamorphosis of laboratory-reared larvae of Concholepas
concholepas (Mollusca; Gastropoda). Aquaculture 126:299–303.
Capo, T. R., A. T. Bardales, P. R. Gillette, M. R. Lara, M. C. Schmale &
J. E. Serafy. 2009. Larval growth, development, and survival of
laboratory-reared Aplysia califonica: effects of diet and veliger
density. Comp. Biochem. Physiol. 149:215–223.
Chester, C. M. 1996. The effect of adult nutrition on the reproduction
and development of the estuarine nudibranch, Tenellia adspersa
(Nordmann, 1845). J. Exp. Mar. Biol. Ecol. 198:113–130.
Chiu, J. M. Y., T. Y. T. Ng, W. X. Wang, V. Thiyagarajan & P. Y. Qian.
2007. Latent effects of larval food limitation on filtration rate,
carbon assimilation and growth in juvenile gastropod Crepidula
onyx.Mar. Ecol. Prog. Ser. 343:173–182.
Cob, Z. C., A. Arshad, J. S. Bujang & M. A. Ghaffer. 2009. Seasonal
variation in growth and survival of Strombus canarium (Linnaeus,
1758) larvae. Pak. J. Biol. Sci. 12:676–682.
Cob, Z. C., A. Arshad, J. S. Bujang, W. L. W. Muda & M. A. Ghaffar.
2010. Metamorphosis induction of the dog conch Strombus cana-
rium (Gastropoda: Strombidae) using cues associated with conch
nursery habitat. J. Appl. Sci. 10:628–635.
Collin, R. 2000. Sex change, reproduction, and development of
Crepidula adunca and Crepidula lingulata (Gastropoda: Calyptraei-
dae). Veliger 43:24–33.
Comtet, T. & P. Riera. 2006.
d
13
C and
d
15
N changes after dietary shift in
veliger larvae of the slipper limpet Crepidula fornicata: an experi-
mental evidence. Helgol. Mar. Res. 60:281–285.
Conroy, P. T., J. W. Hunt & B. S. Anderson. 1996. Validation of a short-
term toxicity test endpoint by comparison with longer-term effects
on larval red abalone Haliotis rufescens.Environ. Toxicol. Chem.
15:1245–1250.
Couper, J. M. & E. M. Leise. 1996. Serotonin injections induce
metamorphosis in larvae of the gastropod mollusc Ilyanassa obso-
leta.Biol. Bull. 191:178–186.
Crim, R. N., J. M. Sunday & C. D. G. Harley. 2011. Elevated seawater
CO
2
concentrations impair larval development and reduce larval
survival in endangered northern abalone (Haliotis kamtschatkana).
J. Exp. Mar. Biol. Ecol. 400:272–277.
Daume, S., A. Krsinich, S. Farrell & M. Gervis. 2000. Settlement, early
growth and survival of Haliotis rubra in response to different algal
species. J. Appl. Phycol. 12:479–488.
Daume, S. & S. Ryan. 2004. Nursery culture of the abalone Haliotis
laevigata: larval settlement and juvenile production using cultured
algae or formulated feed. J. Shellfish Res. 23:1019–1026.
Delgado, G. A., R. A. Glazer & D. Wetzel. 2013. Effects of mosquito
control pesticides on competent Queen Conch (Strombus gigas)
larvae. Biol. Bull. 225:79–84.
Diederich, C. M., J. N. Jarrett, O. R. Chaparro, C. J. Segura, S. M.
Arellano & J. A. Pechenik. 2011. Low salinity stress experienced by
larvae does not affect post-metamorphic growth or survival in three
calyptraeid gastropods. J. Exp. Mar. Biol. Ecol. 397:94–106.
Dobberteen, R. A. & J. A. Pechenik. 1987. Comparison of larval
bioenergetics of two marine gastropods with widely differing lengths
PADILLA ET AL.864
of planktonic life, Thais haemastoma canaliculata (Gray) and
Crepidula fornicata (L.). J. Exp. Mar. Biol. Ecol. 109:173–191.
Eyster, L. S. & J. A. Pechenik. 1988. Comparison of growth, respiration,
and feeding of juvenile Crepidula fornicata (L.) following natural or
KCl-triggered metamorphosis. J. Exp. Mar. Biol. Ecol. 118:269–
279.
Fukazawa, H., H. Takami, T. Kawamura & Y. Watanabe. 2005. The
effect of egg quality on larval period and postlarval survival of an
abalone Haliotis discus hannai.J. Shellfish Res. 24:1141–1147.
Garcia Santaella, E. & D. A. Aranda. 1994. Effects of algal food and
feeding schedule on larval growth and survival rates of the queen
conch, Strombus gigas (Mollusca, Gastropoda), in Mexico. Aqua-
culture 128:261–268.
Gaudette, M. F., J. L. Lowther & J. A. Pechenik. 2001. Heat shock
induces metamorphosis in the larvae of the prosobranch gastropod
Crepidula fornicata.J. Exp. Mar. Biol. Ecol. 266:151–164.
Grubert, M. A. & A. J. Ritar. 2004. The effect of temperature on the
embryonic and larval development of blacklip (Haliotis rubra) and
greenlip (H. laevigata) abalone. Invertebr. Reprod. Dev. 45:197–203.
Grudemo, J. & C. Andr
e. 2001. Salinity dependence in the marine mud
snails Hydrobia ulvae and Hydrobia ventrosa.J. Mar. Biol. Assoc.
U.K. 81:651–654.
Hamel, J. & A. Mercier. 2006. Factors regulating the breeding and
foraging activity of a tropical opisthobranch. Hydrobiologia
571:225–236.
Hamel, J., P. Sargent & A. Mercier. 2008. Diet, reproduction, settlement
and growth of Palio dubia (Nudibranchia: Polyceridae) in the north-
west Atlantic. J. Mar. Biol. Assoc. U.K. 88:365–374.
Hansen, B. & K. W. Ockelmann. 1991. Feeding behaviour in larvae of
the opisthobranch Philine aperta I. Growth and functional response
at different developmental stages. Mar. Biol. 111:255–261.
Hayimad, T., A. B. Abol-Munafi & C. Pitagsalee. 2008. Effect of
different diets on the growth and survival of the larvae and juveniles
of spotted babylon snails (Babylonia areolata Link 1807). J. Sustain.
Sci. Manag. 3:58–65.
Hunt, J. W. & B. S. Anderson. 1989. Sublethal effects of zinc and
municipal effluents on larvae of the red abalone Haliotis rufescens.
Mar. Biol. 101:545–552.
Jackson, D. J., N. Ellemor & B. M. Degnan. 2005. Correlating gene
expression with larval competence, and the effect of age and
parentage on metamorphosis in the tropical abalone Haliotis
asinina.Mar. Biol. 147:681–697.
Jaeckle, W. B. & D. T. Manahan. 1992. Experimental manipulations of
the organic composition of seawater: implications for studies of
energy budgets in marine invertebrate larvae. J. Exp. Mar. Biol.
Ecol. 156:273–284.
Kang, K. H., B. Kim, J. M. Kim & Y. H. Kim. 2003. Effects of amino
acids on larval settlement and metamorphosis in Haliotis discus
hannai.Korean J. Malacol. 19:95–106.
Kay, M. C. 2002. Recruitment in the intertidal limpet Lottia digitalis
(Patellogastropoda: Lottiidae) may be driven by settlement cues
associated with adult habitat. Mar. Biol. 141:467–477.
Klinzing, M. S. E. & J. A. Pechenik. 2000. Evaluating whether velar lobe
size indicates food limitation among larvae of the marine gastropod
Crepidula fornicata.J. Exp. Mar. Biol. Ecol. 252:255–279.
Kritsanapuntu, S., N. Chaitanawisuti & Y. Natsukari. 2007. Effects of
different diet and seawater systems on egg production and quality of
the broodstock Babylonia areolata L. under hatchery conditions.
Aquacult. Res. 38:1311–1316.
Krug, P. J., D. Gordon & M. R. Romero. 2012. Seasonal polyphenism
in larval type: rearing environment influences the development mode
expressed by adults in the sea slug Alderia willowi.Integr. Comp.
Biol. 52:161–172.
Leise, E. M., S. J. Froggett, J. E. Nearhoof & L. B. Cahoon. 2009.
Diatom cultures exhibit differential effects on larval metamorphosis
in the marine gastropod Ilyanassa obsoleta (Say). J. Exp. Mar. Biol.
Ecol. 379:51–59.
Li, A. & J. M. Y. Chiu. 2013. Latent effects of hypoxia on the gastropod
Crepidula onyx.Mar. Ecol. Prog. Ser. 480:145–154.
Lima, G. M. & J. A. Pechenik. 1985. The influence of temperature on
growth rate and length of larval life of the gastropod, Crepidula
plana Say. J. Exp. Mar. Biol. Ecol. 90:55–71.
Lin, K. J., T. P. Chen, T. S. Huang & W. S. Tsai. 2004. Induced
spawning and embryonic development of the top shell, Tectus
pyramis.J. Taiwan Fish. Res. 12:49–60.
Liu, L., L. Chu & K. Chang. 1986. Negative effect of g-aminobutyric
acid (GABA) on the settlement of larvae of the small abalone,
Haliotis diversicolor supertexta Lischke. Bull. Inst. Zool. Acad. Sin.
25:1–5.
Lu, J. Y., Q. Lin, Y. Y. Sun, J. Q. Sheng & Q. X. Chen. 2004. Effect of
temperature on the early development of Haliotis diversicolor Reeve.
J. Shellfish Res. 23:963–966.
Lucas, J. S. & J. D. Costlow. 1979. Effects of various temperaturecycles
on the larval development of the gastropod mollusc Crepidula
fornicata.Mar. Biol. 51:111–117.
Maldonado, R., A. M. Ibarra, J. L. Ram
ırez, S. Avila, J. E. V
azquez &
L. M. Badillo. 2001. Induction of triploidy in pacific red abalone
(Haliotis rufescens). J. Shellfish Res. 20:1071–1075.
Manzano, B. N., D. A. Aranda & E. B. C
ardenas. 1999. Development,
growth and survival of larvae of the fighting conch Strombus pugilis
L. (Mollusca, Gastropoda) in the laboratory. Bull. Mar. Sci. 64:201–
208.
Marty, R., N. Desroy, S. Bureau & C. Reti
ere. 2003. Relationship
between density and feeding frequency for reared larvae of the
gastropod Crepidula fornicata.J. Mar. Biol. Assoc. U.K. 83:499–500.
McGee, B. L. & N. M. Targett. 1989. Larval habitat selection in
Crepidula (L.) and its effect on adult distribution patterns. J. Exp.
Mar. Biol. Ecol. 131:195–214.
Mestre, N. C., A. Brown & S. Thatje. 2013. Temperature and pressure
tolerance of larvae of Crepidula fornicata suggest thermal limitation
of bathymetric range. Mar. Biol. 160:743–750.
Miller, S. E. & M. G. Hadfield. 1986. Ontogeny of phototaxis and
metamorphic competence in larvae of the nudibranch Phestilla
sibogae Bergh (Gastropoda: Opisthobranchia). J. Exp. Mar. Biol.
Ecol. 97:95–112.
Morse, D. E., H. Duncan, N. Hooker, A. Baloun & G. Young. 1980.
GABA induces behavioral and developmental metamorphosis in
planktonic molluscan larvae. Fed. Proc. 39:3237–3241.
Noble, W. J., K. Benkendorff & J. O. Harris. 2015. Growth, settlement
and survival of Dicathais orbita (Neogastropoda, Mollusca) larvae
in response to temperature, diet and settlement cues. Aquacult. Res.
46:1455–1468.
Padilla, D. K., M. J. McCann, M. McCarty Glenn, A. P. Hooks &
S. E. Shumway. 2014. Effect of food on metamorphic competence in
the model system Crepidula fornicata.Biol. Bull. 227:242–251.
Park, C., Q. Li, T. Kobayashi & A. Kijima. 2006. Inbreeding depression
traits in Pacific abalone Haliotis discus hannai by factorial mating
experiments. Fish. Sci. 72:774–780.
Pechenik, J. A. 1980. Growth and energy balance during the larval lives
of three prosobranch gastropods. J. Exp. Mar. Biol. Ecol. 44:1–28.
Pechenik, J. A. 1984. The relationship between temperature, growth
rate, and duration of planktonic life for larvae of the gastropod
Crepidula fornicata (L.). J. Exp. Mar. Biol. Ecol. 14:241–257.
Pechenik, J. A., D. E. Cochrane, W. Li, E. T. West, A. Pires &
M. Leppo. 2007. Nitric oxide inhibits metamorphosis in larvae of
Crepidula fornicata, the slippershell snail. Biol. Bull. 213:160–171.
Pechenik, J. A. & L. S. Ester. 1989. Influence of delayed metamorphosis
on the growth and metabolism of young Crepidula fornicata
(Gastropoda) juveniles. Biol. Bull. 176:14–24.
Pechenik, J. A., M. S. Estrella & K. Hammer. 1996a. Food limitation
stimulates metamorphosis of competent larvae and alters postme-
tamorphic growth rate in the marine prosobranch gastropod
Crepidula fornicata.Mar. Biol. 127:267–275.
GASTROPOD LARVAL DEVELOPMENT 865
Pechenik, J. A. & C. C. Gee. 1993. Onset of metamorphic competence in
larvae of the gastropod Crepidula fornicata (L.), judged by a natural
and artificial cue. J. Exp. Mar. Biol. Ecol. 167:59–72.
Pechenik, J. A., T. Gleason, D. Daniels & D. Champlin. 2001. Influence
of larval exposure to salinity and cadmium stress on juvenile
performance of two marine invertebrates (Capitella sp. I and
Crepidula fornicata). J. Exp. Mar. Biol. Ecol. 264:101–114.
Pechenik, J. A., K. Hammer & C. Weise. 1996b. The effect of starvation
on acquisition of competence and post-metamorphic performance in
the marine prosobranch gastropod Crepidula fornicata (L.). J. Exp.
Mar. Biol. Ecol. 199:137–152.
Pechenik, J. A. & W. D. Heyman. 1987. Using KCI to determine size at
competence for larvae of the marine gastropod Crepidula fornicata
(L.). J. Exp. Mar. Biol. Ecol. 112:27–38.
Pechenik, J. A., T. J. Hilbish, L. S. Eyster & D. Marshall. 1996c.
Relationship between larval and juvenile growth rates in two marine
gastropods, Crepidula plana and Crepidula fornicata.Mar. Biol.
125:119–127.
Pechenik, J. A., J. N. Jarrett & J. Rooney. 2002a. Relationships between
larval nutritional experience, larval growth rates, juvenile growth
rates, and juvenile feeding rates in the prosobranch gastropod
Crepidula fornicata.J. Exp. Mar. Biol. Ecol. 280:63–78.
Pechenik, J. A. & S. H. Levine. 2007. Estimates of planktonic larval
mortality using the marine gastropods Crepidula fornicata and
Crepidula plana.Mar. Ecol. Prog. Ser. 344:107–118.
Pechenik, J. A. & G. M. Lima. 1984. Relationship between growth,
differentiation, and length of larval life for individually reared larvae
of the marine gastropod, Crepidula fornicata.Biol. Bull. 166:537–
549.
Pechenik, J. A. & A. S. Tyrell. 2015. Larval diet alters larval growth
rates and post-metamorphic performance in the marine gastropod
Crepidula fornicata.Mar. Biol. 162:1597–1610.
Pechenik, J. A., L. Wei & D. E. Cochrane. 2002b. Timing is everything:
the effects of putative dopamine antagonists on metamorphosis vary
with larval age and experimental duration in the prosobranch
gastropod Crepidula fornicata.Biol. Bull. 202:137–147.
Pena, J. B. 1985. The culture of Haliotis discus Reeve (Gastropoda;
Prosobranchia) from fertilization to one-year-old in laboratory
conditions. Iberus 5:21–30.
Penniman, J. R., M. K. Doll & A. Pires. 2013. Neural correlates of
settlement in veliger larvae of the gastropod, Crepidula fornicata.
Invertebr. Biol. 132:14–26.
Pereira, L., J. Lagos & F. Araya. 2007. Evaluation of three methods for
transporting larvae of the red abalone Haliotis rufescens Swainson
for use in remote settlement. J. Shellfish Res. 26:777–781.
Perron, F. E. 1981. Larval growth and metamorphosis of Conus
(Gastropoda: Toxoglossa) in Hawaii. Pac. Sci. 35:25–38.
Phillips, N. E. 2011. Where are larvae of the vermetid gastropod
Dendropoma maximum on the continuum of larval nutritional
strategies? Mar. Biol. 158:2335–2342.
Pilkington, M. C. & J. B. Pilkington. 1984. The stimulus for meta-
morphosis of a high-shore pulmonate, Amphibola crenata.J. R. Soc.
N. Z. 14:139–143.
Pillsbury, K. S. 1985. The relative food value and biochemical compo-
sition of five phytoplankton diets for queen conch, Strombus gigas
(Linne) larvae. J. Exp. Mar. Biol. Ecol. 90:221–231.
Pires, A. & M. G. Hadfield. 1991. Oxidative breakdown products of
catecholamines and hydrogen peroxide induce partial metamorpho-
sis in the nudibranch Phestilla sibogae Bergh (Gastropoda: Opistho-
branchia). Biol. Bull. 180:310–317.
Pires, A. & M. G. Hadfield. 1993. Responses of isolated vela of
nudibranch larvae to inducers of metamorphosis. J. Exp. Zool.
266:234–239.
Raimondi, P. T., A. M. Barnett & P. R. Krause. 1997. The effects of
drilling muds on marine invertebrate larvae and adults. Environ.
Toxicol. Chem. 6:1218–1228.
Richmond, C. E. & S. A. Woodin. 1999. Effect of salinity reduction on
oxygen consumption by larval estuarine invertebrates. Mar. Biol.
134:259–267.
Roberts, R. D., H. F. Kaspar & R. J. Barker. 2004. Settlement of
abalone (Haliotis iris) larvae in response to five species of coralline
algae. J. Shellfish Res. 23:975–987.
Roberts, R. D., T. Kawamura & C. M. Handley. 2007. Factors affecting
settlement of abalone (Haliotis iris) larvae on benthic diatoms films.
J. Shellfish Res. 26:323–334.
Roberts, R. D., T. Kawamura & C. M. Nicholson. 1999. Growth and
survival of postlarval abalone (Haliotis iris) in relation to develop-
ment and diatom diet. J. Shellfish Res. 18:243–250.
Roberts, R. D., C. Lapworth & R. J. Barker. 2001. Effect of starvation
on the growth and survival of post-larval abalone (Haliotis iris).
Aquaculture 200:323–338.
Roberts, R. D. & C. M. Nicholson. 1997. Variable response from
abalone larvae (Haliotis iris,H. virginea) to a range of settlement
cues. Molluscan Res. 18:131–141.
Roberts, R. D. & E. Watts. 2010. Settlement of Haliotis australis larvae:
role of cues and orientation of the substratum. J. Shellfish Res.
29:663–670.
Rodriguez, S. R., C. Riquelme, E. O. Campos, P. Chavez, E. Brandan &
N. C. Inestrosa. 1995. Behavioral responses of Concholepas con-
cholepas (Brugui
ere, 1798) larvae to natural and artificial settlement
cues and microbial films. Biol. Bull. 189:272–279.
Romero, M. R., K. M. Walker, C. J. Cortez, Y. Sanchez, K. J. Nelson,
D. C. Ortega, S. L. Smick, W. J. Hoese & D. C. Zacherl. 2012. Larval
diel vertical migration of the marine gastropod Kelletia kelletii
(Forbes, 1850). J. Mar. Biol. 2012:1–9.
Santaella, E. G. & D. A. Aranda. 1994. Effect of algal food and feeding
schedule on larval growth and survival rates of the queen conch,
Strombus gigas (Mollusca, Gastropoda), in Mexico. Aquaculture
128:261–268.
Sawatpeera, S., M. Kruatrachue, P. Sonchaeng, S. Upatham &
T. Rojanasarampkit. 2004. Settlement and early growth of abalone
larvae Haliotis asinine Linnaeus in response to presence of diatoms.
Veliger 47:91–99.
Schlesinger, A., R. Goldshmid, M. G. Hadfield, E. Kramarsky-Winter &
Y. Loya. 2009. Laboratory culture of the aeolid nudibranch Spurilla
neopolitana (Mollusca, Opisthobranchia): life history aspects.
Mar. Biol. 156:753–761.
Searcy-Bernal, R. & C. Anguiano-Beltr
an. 1998. Optimizing the
concentration of gamma-aminobutyric acid (GABA) for inducing
larval metamorphosis in the red abalone Haliotis rufescens (Mollusca:
Gastropoda). J. World Aquacult. Soc. 29:463–470.
Searcy-Bernal, R., A. E. Salas-Garza, R. A. Flores-Aguilar & P. R.
Hinojosa-Rivera. 1992. Simultaneous comparison of methods for
settlement and metamorphosis induction in the red abalone (Hal-
iotis rufescens). Aquaculture 105:241–250.
Seelemann, U. 1967. Rearing experiments on the amphibian slug
Alderia modesta.Helgoland. Wiss. Meer. 15:128–134.
Shaojun,B.,Z.Tao,P.Hengqian,P.Yang,W.Pingchuan&
X. Dongxiu. 2014. Effects of temperature and salinity on the devel-
opment of embryos and larvae of the veined rapa whelk Rapana
venosa (Valenciennes, 1846). Chin. J. Oceanology Limnol. 32:773–782.
Shen, Y. L., J. T. Huang, X. P. Ge, A. M. Wang, F. Lv, W. C. Cai &
N. N. Shen. 2013. Effects of different hatching ways, cultivating
densities and incubators on the artificial breeding of Onchidium
struma.Mar. Sci. 37:109–116.
Shieh, H. & L. Liu. 1999. Positive effects of large concentration in
culture on the development of the lecithotrophic larvae of Babylonia
formosae (Sowerby) (Prosobranchia: Buccinidae). J. Exp. Mar. Biol.
Ecol. 241:97–105.
Sisson, C. D. 2002. Dichotomous life history patterns for the nudi-
branch Dendronotus frondosus (Ascanius, 1774) in the Gulf of
Maine. Veliger 45:290–298.
PADILLA ET AL.866
Slattery, M. 1992. Larval settlement and juvenile survival in the red
abalone (Haliotis rufescens)—an examination of inductive cues and
substrate selection. Aquaculture 102:143–153.
Stoner, A. W., M. Ray, R. A. Glazer & K. J. McCarthy. 1996.
Metamorphic responses to natural substrata in a gastropod larva:
decisions related to postlarval growth and habitat preference.
J. Exp. Mar. Biol. Ecol. 205:229–243.
Stott, A. E., T. Takeuchi & Y. Koike. 2004. An alternative culture
system for the hatchery production of abalone without using live-
food. Aquaculture 236:341–360.
Struhsaker, J. W. & J. D. Costlow. 1969. Some environmental effects on
the larval development of Littorina picta (Mesogastropoda), reared
in the laboratory. Malacologia 9:403–419.
Taris, N., T. Comtet, R. Stolba, R. Lasbleiz, J. A. Pechenik & R. Viard.
2010. Experimental induction of larval metamorphosis by a natu-
rally-produced halogenated compound (dibromomethane) in the
invasive mollusc Crepidula fornicata (L.). J. Exp. Mar. Biol. Ecol.
393:71–77.
Teng, W., X. Wu, B. Tang, Y. Cheng, B. Zhou, J. Wang, J. Wang &
Y. Chen. 2007. The study of ecological reproduction of Onchidium
struma in wetland. Mar. Fish. 29:1004–2490.
Todd,C.D.,M.G.Bentley&J.N.Havenhand.1991.Larval
metamorphosis of the opisthobranch mollusc Adalaria proxima
(Gastropoda: Nudibranchia): the effects of choline and elevated
potassium ion concentration. J. Mar. Biol. 71:53–72.
Trowbridge, C. D. 1998. Stenophagous, herbivorous sea slugs attack
desiccation-prone, green algal hosts (Codium spp.): indirect evidence
of prey-stress models (PSMs)? J. Exp. Mar. Biol. Ecol. 230:31–53.
Untersee, S. & J. A. Pechenik. 2007. Local adaptation and maternal
effects in two species of marine gastropod (genus Crepidula) that
differ in dispersal potential. Mar. Ecol. Prog. Ser. 347:79–85.
Ushakova, O. O. & O. L. Saranchova. 2003. Low salinity resistance of
plankton larvae in invertebrates (Polychaeta, Gastropoda, Echino-
dermata, and Bryozoa) from the White Sea. Zool. Zh. 82:318–324.
Vargas, C. A., M. De la Hoz, V. Aguilera, V. San Mart
ın, P. H.
Manr
ıquez, J. M. Navarro, R. Torres, M. A. Lardies & N. A. Lagos.
2013. CO
2
—driven ocean acidification reduces larval feeding effi-
ciency and changes food selectivity in the mollusk Concholepas
concholepas.J. Plankton Res. 35:1059–1068.
Vargas, C. A., P. H. Manriquez & S. A. Navarrete. 2006. Feeding by
larvae of intertidal invertebrates: assessing their position in pelagic
food webs. Ecology 87:444–457.
Yang, Z., X. Zhang & Z. Cai. 2009. Toxic effects of several phthalate
esters on the embryos and larvae of abalone Haliotis diversicolor
supertexta.Chin. J. Oceanology Limnol. 27:395–399.
Yaroslawseva, L. M. & E. P. Sergeeva. 2008. Adaptive abilities of
marine invertebrate larvae under changes in environmental factors
as sensitive test for sea water pollution. Biologiia Moria 34:42–46.
Zhao, B., J. Qiu & P. Qian. 2003. Effects of food availability on larval
development in the slipper limpet Crepidula onyx (Sowerby). J. Exp.
Mar. Biol. Ecol. 294:219–233.
Zheng, H., C. Ke, S. Zhou & F. Li. 2005. Effects of starvation on larval
growth, survival and metamorphosis of ivory shell Babylonia
formosae habei Altena et al., 1981 (Neogastropoda: Buccinidae).
Aquaculture 243:357–366.
Zimmerman, K. M. & J. A. Pechenik. 1991. How do temperature and
salinity affect relative rates of growth, morphological differentia-
tion, and time to metamorphic competence in larvae of the marine
gastropod Crepidula plana?Biol. Bull. 180:372–386.
Zippay, M. L. & G. E. Hoffman. 2010. Effect of pH on gene expression
and thermal tolerance of early life history stages of red abalone
(Haliotis rufescens). J. Shellfish Res. 29:429–439.
GASTROPOD LARVAL DEVELOPMENT 867
ResearchGate has not been able to resolve any citations for this publication.
Article
Full-text available
Larvae of the marine gastropod Crepidula fornicata must complete a transition from the plankton, where they are highly dispersed, to an aggregated group of benthic adults. Previous research has shown that selective settlement of larvae on conspecific adults is mediated by a water-borne chemical cue. However, variable experimental conditions have been used to study this cue, and standardization is needed in order to investigate factors that may have weak effects on settlement. In this study, we developed a time-course bioassay based on a full-factorial design with temporal blocking and statistical analysis of larval settlement rates in the lab. We tested this bioassay by examining settlement in the presence of an abiotic cue (KCl), and biotic cues (water conditioned with adult conspecifics and conspecific pedal mucus). Results confirmed settlement in the presence of both KCl and adult-conditioned water, and discovered the induction of settlement by pedal mucus. This optimized, standardized bioassay will be used in future experiments to characterize the complex process of larval settlement in C. fornicata , particularly to measure components of potentially small effect.
Article
Full-text available
Diatoms are the principal food source for the abalone larvae before switching to eat macroalgae, but most of the diatoms culture systems rely on naturally occurring diatom species to supply live feed to juveniles. Monostrains of Navicula incerta Grunow and Grammatophora marina Ehrenberg benthic diatoms were cultured on wavy plastic plates (so called "Papan") in the laboratory. The settlement of abalone larvae and growth of abalone spat were compared with using diatoms live feed of N. incerta monostrain (NIM), G. marina monostrain (GMM) and wild mixed strains in the abalone hatchery. Benthic diatom abundances on papan of NIM, GMM, and WMS were 6.71 x10(5), 7.01x10(5) and 7.56x10(5) cells (cm(2) surf.)(-1) at the beginning of the experiment, whereas at the end, the abundances had decreased to 2.75x10(3), 2.84x10(3), and 3.31x10(3) cells (cm(2) surf.)(-1), respectively. Initially, NIM and GMM diatoms occupied 95.4% and 96.8%, respectively, of the benthic diatom community, which decreased to 69.8% and 65.5% by the end of the experiment. The average number of settled juvenile abalone was 1000, 1080, and 640 in the tank where the live feed was NIM, GMM and WMS, respectively. Survival rates of juvenile abalone were 2.00, 2.16, and 1.28% in the tank of NIM, GMM and WMS, respectively. The specific growth rates of juvenile abalone were 3.28, 3.07, and 2.92% in tanks with NIM, GMM, and WMS, respectively. The average live feed consumption rate by each abalone per day was 0.17, 0.15, and 0.26% of the benthic diatom standing crop in cultures of NIM, GMM, and WMS, respectively. In conclusion, mono-strain benthic diatoms exhibited higher settlement and growth of abalone larvae than did cultures of a wild mixed strain.
Article
Full-text available
Some larval experiences can produce “latent effects” on post-metamorphic growth or survival. While it is known that periods of starvation during larval development can cause such latent effects, the effect of larval diet on post-metamorphic growth has not been studied. As global climate change and ocean acidification are expected to decrease phytoplankton concentrations and alter both phytoplankton species composition and nutritional characteristics, we examined the impact of 3 phytoplankton species (Isochrysis galbana, clone T-ISO; Pavlova lutheri, clone MONO; and Dunaliella tertiolecta, clone DUN) on larval growth and subsequent post-metamorphic fitness in the slippersnail Crepidula fornicata. Once larvae metamorphosed, the juveniles were all reared on the diet that produced the fastest growth, T-ISO, to look for latent effects of larval diet on juvenile growth. In all experiments, larvae grew most quickly on T-ISO; diet did not affect relative rates of shell and tissue growth. In 2 of the 4 experiments conducted on the effects of diet quality, larvae reared on T-ISO metamorphosed into juveniles that grew significantly faster than those that had been raised on the other phytoplankton species, indicating clear latent effects of dietary experience and suggesting parent-related genetic variation in susceptibility to this type of stress. Rearing larvae at a very low food concentration of T-ISO (1 × 104 cells ml−1) until metamorphosis also produced severe latent effects on juvenile growth, reducing juvenile growth rates by more than 30 %. These data provide yet another example of how stresses experienced during larval development can influence post-metamorphic performance, and add another level of complexity to attempts at predicting the future consequences of environmental change on marine community structure and species interactions.
Article
Laboratory experiments were conducted to test the adaptive significance of settlement and metamorphosis responses in competent veligers of Strombus gigas Linnaeus (queen conch). When competent veligers were tested for metamorphic response to 15 substrata collected from nursery grounds in seagrass beds of the Florida Keys, 0-38% underwent metamorphosis. Substrata with complex physical and biotic structures such as the calcareous red alga Neogoniolithon strictum (Foslie) Setchell and Mason, the green alga Dasycladus vermicularis (Scopoli) Krasser, and the matrix of algae and sediment attached to rock substrata elicited highest responses. No larvae responded to live blades of the seagrasses Thalussia testudinum Koenig and Syringodium jilifome Kuetzing, indicating that these plants are not the primary inducement for recruitment of conch to seagrass meadows. When newly-settled conch were grown for 16 days on the same substrata used to test for metamorphic responses, growth rates ranged from 7-62 pm/day and were weakly correlated (r = 0.71) with frequency of metamorphosis. High growth rates were associated with substrata that elicited high, low, or no metamorphic responses (e.g.. on Thalassia testudinum), but low growth was always associated with low metamorphosis. High metamorphosis occurred with substrata that were preferred as habitat by postlarval conch and yielded high growth rates. Settlement decisions by queen conch larvae appear to have important adaptive significance for newly metamorphosed recruits.
Article
The low salinity resistance of competent pelagic larvae in some invertebrate species (Polychaeta, Gastropoda, Echinodermata, and Bryozoa) from the White Sea was studied in laboratory experiments. The flucluations of salinity within a range of 8 to 12‰ affect to a great extent the survivorship and matamorphosis of the invertebrate larvae. Two groups of species, whose resistance to salinity differed according to the results obtained and the calculated lethal dose (LD50), were distinguished. The high resistance of larvae in different systematic groups of invertebrates in the White Sea should be considered as their ecological adaptation to the specific hydrological regime of this sea. Probably, this high adaptive ability of larvae reflects a potential ecological niche of the species.
Article
GABA (gamma-aminobutyric acid) of different concentrations (10 -6, 10-5, 10-4, 10-3 M) was tested for its effects on the settlement response of abalone Haliotis asinina larvae of 48 hours old. The highest percentage (73.5%) of attachment was found in larvae reared in seawater containing 10-6 M GABA. In addition, five benthic diatom species (Navicula sp. 1, Navicula sp. 2, Navicula sp. 3, Nitzschia sp. 1, and Nitzschia sp. 2) were isolated and maintained in culture. The species were grown in small bowls and tested in settlement experiments with H. asinina larvae. Settlement was very high in 2-day-old larvae fed five species of diatoms (89.8-94.3%). Survival rates declined when the larvae were older (6-7 days). The highest percentages of metamorphosis and shell growth were found in larvae fed Navicula sp. 1, Nitzschia sp. 2, and Navicula sp. 1. A flow-through system in large fiberglass tanks was developed to compare growth and survival of postlarvae reared on diatoms, Navicula sp. 1, Navicula sp. 2, and Nitzschia sp. 1 for 120 days. The shell length (SL) and weight (W) of postlarvae were measured once every 2 weeks. The best growth rate was obtained with postlarvae fed Nitzschia sp. 1 (SL 81.7 μm/day, W 96.7 μg/day) and Navicula sp. 2 (SL 75.0 μm/day, W 78.3 μg/day).
Article
The nudibranch Dendronotus frondosus has a wide distribution and different morphological, ecological, and life history traits within its range. In the Gulf of Maine, populations can be found with either lecithotrophic or planktotrophic veliger larvae. Adults with these two types of larvae have overlapping habitat distributions, but the veligers differ in size, basic developmental characteristics, and composition of gelatinous clutches. Seasonal patterns of size distribution of adults suggest a sub-annual life cycle for those with planktotrophic larvae and an annual life cycle for those with lecithotrophic larvae. A feeding experiment with two types of hydroid prey resulted in lower growth rates for one dietary treatment, although this did not result in a shift in larval type. Mating recognition trials suggest a behavioral reproductive isolating mechanism between some populations. These results show little evidence for poecilogony and are motive for a taxonomic review of a D. frondosus complex in the Gulf of Maine.
Article
Postlarval abalone (Haliotis iris) were reared on five unialgal diatom diets from 3 to 68 days postsettlement. Diatom strain affected both survival and growth, which were positively correlated (r = 0.88, p = 0.05, n = 5). The digestibility and ingestibility of diatoms were both important. Survival ranged from low (<10% on day 37 postsettlement) on Pleurosigma sp. diet, to high (>70% on day 68) on Cocconeis scutellum, Cylindrotheca closterium; and Navicula ramosissima diets. Diet had little effect on growth and survival in the first 16 days after settlement, provided postlarvae were ingesting adequate food. Growth rates during the week to day 10 were relatively high (means of 20-29 μm shell length per day). Growth rates from days 10 to 16 were lower than in the first week (t = 7.33, p < 0.001) and again similar among all diets (means 15-20 μm/day) except Pleurosigma sp. (2 μm/day), which was not ingested by larvae <1 mm shell length. After day 17, postlarvae grew fastest on the strains that were most efficiently digested (C. scutellum and C. Closterium). The digestion efficiency of two diatom strains increased markedly during the experiment; because of changes in diatom condition. Postlarvae were feeding on small diatoms (12 X 4 X 3 μm) by day 2 postsettlement, and digestive gland development became visible on day 3. Fecal volume increased approximately cubically in relation to shell length, indicating rapidly increasing food consumption.
Article
Abalone recruits are found predominantly on crustose coralline algae (CCA) and recruitment seems to vary among coralline species or growth-forms. Spatial patterns in the recruitment of marine invertebrates can be formed by processes acting before. during. or after settlement. This Study used laboratory experiments to examine the settlement of Haliotis iris larvae on five species of CCA. When the CCA species were presented individually to larvae, all induced > 88% of larvae to attach within 1 day, and > 80% to metamorphose within 3 days. When given a choice of the five CCA, larvae settled most on Pneophyllum coronetum and Hydrolithon rupestris, and settled least on Mesophyllum printzianum. Phymatolithon repandum, and Lithophyllum carpophylli gave intermediate results. The speed of metamorphosis in the no-choice experiments mirrored the species preferences in the choice experiments, with metamorphosis occurring most rapidly on Pneophvllum coronatum and Hydrolithon rupestris. The two preferred species were thin crusts. whereas the two least preferred species formed thick, morphologically complex crusts. In a choice experiment, the proportion of larvae choosing a CCA specimen showed no correlation with bacterial density (r = -0.25, P = 0.52, n = 25), but a weak positive correlation with diatom density (r = 0.52, P = 0.02, n = 25). However, diatom densities were low on all CCA species, and are unlikely to be a primary cause of settlement preference. It is hypothesized that Lit least some of the variation in recruitment among CCA species or growth forms observed in the wild is determined by selective settlement.