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Expedition Report
CSU-LSAMP * Costa Rica Research Program
Summer 2012
Edited by
Diana Lieberman & Sheldon Leiker
California State University Monterey Bay
Seaside, CA 93955 USA
CSU-LSAMP is funded through the National Science Foundation (NSF) under grant #HRD-0802628 and the Chancellor's Office of the California State University. Any opinions, findings, and conclusions or recommendations expressed in this
material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation or the Chancellor's Office of the CSU.
Programmatic funding for the Costa Rica Summer Research Project was also made available by CSU Monterey Bay’s SEP.org grant incentive program for the Division of Science & Environmental Policy.
.
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Table of Contents
Acknowledgements..............................................................................................................................4
Program Participants............................................................................................................................5
Program Overview...............................................................................................................................9
Details of Study Sites....................................................................................................... ...................10
Maps....................................................................................................................................................11
Program Itinerary...............................................................................................................................12
Research Reports ...............................................................................................................................13
Shell utilization by tropical hermit crabs under strongly contrasting levels of
protection and accessibility. Antonia Estevez-Olea, Alejandro Rios, Adrienne Blaylock
& Philip Schotte ...............................................................................................................14
Analysis of sediments carried by a tropical intertidal sea cucumber, Holothuria inornata, on the Pacific coast of Costa Rica. Mark Jackson, Kara Nygaard &
Areli Tejeda ......................... .................. ...........................................................................42
Comparison of protected and exploited tooth shell (Nerita scabricosta) populations on
the Pacific coast of Costa Rica. Jennifer Retana, Emily Escobar & Dwayne Franco....61
Habitat preference of the intertidal frillfin Bathygobius (Gobiidae) in Cabo Blanco
Absolute Reserve, Costa Rica. Jacob Barrett, Nathaniel Bell, Danielle Kuperus
& Kathleen Sowul ..............................................................................................................95
Comparison of biomechanical properties of hermit crabs using contrasting shell types
on a tropical shore. Amie Nowacki, Adrianna Hernandez & Carlos de la Parra. .....108
Biodiversity: Summary Classification of Living Things Observed by Participants....................133
Gastropod Sightings.........................................................................................................................135
Reptile and Amphibian Sightings...................................................................................................136
Mammal Sightings...........................................................................................................................137
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Bird Sightings....................................................................................................................................138
Fish Sightings....................................................................................................................................140
Personal “Firsts” – new experiences ...............................................................................................142
Cultural Immersion & Homestay Experiences................................................................................143
Photographs...............................................................................................................................146-159
* Homestays, cultural immersion (2) * Class, lab, field * Research (3) * Plants, invertebrates *
* Vertebrates * Travel (2) * Fun (2) * San Miguel Biological Station * Group photo *
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Acknowledgements
Sincere thanks are due to the many faculty and staff members of the California State University
system whose enthusiastic and creative efforts brought this program into being. Preliminary
conversations with CSUMB faculty members Sharon Anderson, Dan Fernandez, Corey Garza, Doug
Smith, Aparna Sreenivasan, and Suzy Worcester were crucial and set the stage for what has followed.
We are especially grateful to Jessica Brown, Bill Head, and Bobby Quiñonez of the UROC office at
CSUMB and Minnie Chabot of CSU Sacramento for their energetic and effective administrative
support. Heartfelt appreciation as well to the LSAMP advisors and mentors throughout the CSU
system who brought this opportunity to the attention of their students and advisees and encouraged
them to apply.
We thank all those who cared for us with such grace and dedication at Hotel Cacts in San Jose and at
the San Miguel Biological Station in Reserva Natural Absoluta Cabo Blanco (MINAET). The staff,
cooks, and community friends at both sites enriched the experience in so many ways and made our
time in Costa Rica productive and enjoyable.
To the families in the community of San Luis de Monteverde who welcomed us into their homes,
generously shared fun, food, and family with us, and made our introduction to Costa Rican culture so
memorable, we are profoundly grateful. Abrazos to the families of Aidee Méndez and Misael
Alvarado; Marina Zamora and Miguel Fuentes; Yenny Cruz; Ofelia Rodriguez; Flory Bogantes and
Carlos Fuentes; Marielos Cruz and Olivier Garro; Damaris Salazar and William Leitón; Virginia
Leitón; Zaida Villalobos; Lita Rodriguez and Koki Fuentes; Edith Salazar and Milton Brenes; Miriam
Salazar; Anabelli Picado and Tino Pérez; Lila Mora and Hugo Picado; Eliza Mata and Alvaro Vega;
Lorena Leitón and Marcos Marín; Liliam Arce and Rafa Leitón; Cristina Obando and Geovanny
Leitón; Tema Salazar and Victor Manuel “Macho” Leitón; and Elvira Cruz and Lelo Mata.
Support for this program was provided through the Chancellor´s Office of the California State
University and NSF grant HRD-0802628 from the LSAMP program of the National Science
Foundation. Programmatic funding was also made available by CSU Monterey Bay’s SEP.org grant
incentive program for the Division of Science & Environmental Policy.
Finally, the participants and staff of the program kindly shared their photographs, field notes, wildlife
sightings, journal entries, reflections, and original research for use in this volume.
Muchisimas gracias a todos y todas / Many thanks to all!
5
Program Participants
Name Major; minor Home campus Email address
Students
Jacob Barrett Chemistry Sonoma [email protected]
Nate Bell Biomed; Chemistry Sacramento [email protected]
Adrienne Blaylock Cell Biology East Bay [email protected]
Juan Carlos de la Parra Engineering San Luis Obispo [email protected]
Emily Escobar Biology; Spanish San Bernardino [email protected]
Antonia Estevez Engineering San Luis Obispo [email protected]
Dwayne Franco Env. Science,
Techol. Policy Monterey Bay [email protected]
Adrianna Hernandez Biology Los Angeles [email protected]
Mark Jackson* Wildlife Biology U. Montana [email protected]
Danielle Kuperus* Biology Minnesota State U. [email protected]
Amie Nowacki* Biology Minnesota State U. [email protected]
Kara Nygaard* Biology Minnesota State U. [email protected]
Jennifer Retana Envir. Engineering Los Angeles [email protected]
Alex Rios
Biology Monterey Bay [email protected]
Katie Sowul Env. Science,
Technol. Policy Monterey Bay [email protected]
Areli Tejeda Cell & Molecular
Biology Channel Islands [email protected]
*NOTE: Participation by Jackson, Kuperus, Nowacki and Nygaard was funded independently, not through the
LSAMP program; the other twelve students were supported by LSAMP funds.
6
Faculty, Staff and Resource Persons
Diana Lieberman Science & Env.
Policy Monterey Bay [email protected]
Milton Lieberman Tropical Ecology,
Marine Biology
Cabo Blanco Absolute
Reserve, Costa Rica [email protected]
Corey Garza Science & Env.
Policy Monterey Bay [email protected]
Sheldon Leiker Science & Env.
Policy Monterey Bay [email protected]
Dean Philpot Marine &
Freshwater Biology University of Newcastle [email protected]
Phillip Schotte Biology Minnesota State U. [email protected]
Oscar Fennell Ornithology Monteverde, Costa Rica [email protected]
7
Program Participants
Students
Jacob Barrett Nate Bell Adrienne Blaylock Carlos de la Parra
CSU Sonoma CSU Sacramento CSU East Bay Cal Poly San Luis Obispo
Emily Escobar Antonia Estevez Dwayne Franco Adrianna Hernandez
CSU San Bernardino Cal Poly San Luis Obispo CSU Monterey Bay CSU Los Angeles
Mark Jackson * Danielle Kuperus * Amie Nowacki * Kara Nygaard *
University of Montana Minn State-Moorhead Minn State-Moorhead Minn State-Moorhead
Jennifer Retana Alex Rios Katie Sowul Areli Tejeda
CSU Los Angeles CSU Monterey Bay CSU Monterey Bay CSU Channel Islands
8
Program Faculty, Staff and Resource Persons
Diana Lieberman, Ph.D. Milton Lieberman, Ph.D.
Division of Science & Environmental Policy Director, San Miguel Biological Station
California State University Monterey Bay Cabo Blanco Absolute Reserve (MINAET)
Sheldon Leiker Dean Philpot Phil Schotte
Teaching Assistant Teaching Assistant Teaching Assistant
CSUMonterey Bay University of Newcastle Minnesota State-Moorhead
Oscar Fennell Araya
Asociacion de Guias Naturalistas
Reserva Bosque Nuboso Monteverde
9
Program Overview
The CSU-LSAMP Costa Rica Research Program is an intensive, interdisciplinary tropical field
program for undergraduates. The primary goals of the program are acquiring proficiency in tropical
natural history; developing skills in observation, critical thinking and analysis; building experience in
design and execution of original research; and growth in global perspectives, adaptability, and self-
reliance.
Summer 2012 participants spent seven weeks at field sites in Costa Rica. Only 1/8 the size of the state
of California, Costa Rica is home to some half a million species—about 4% of the species on the
planet. With around 27% of its area set aside in national parks and reserves, and an estimated 5%
more under protection in a network of private reserves and biological corridors, Costa Rica has a
well-deserved reputation as a world superpower in conservation.
From 10 June-25 July 2012, participants were immersed in the rigorous study of tropical
environments and biological diversity; statistics and research methods; current issues in conservation;
and Costa Rican geography and culture. Approaches to learning on the program included lectures in
the classroom, laboratory, and field; visits to parks and reserves; guided hikes through a diversity of
tropical habitats; various field activities; group discussions; hands-on laboratory studies; cultural
immersion through homestays and social interaction with Costa Ricans from many walks of life; and
research projects and analysis of data.
The program began in the capital city, San Jose, with 3 days of orientation activities, cultural
workshops and introductory lectures. The group then traveled over the continental divide to San
Luis de Monteverde, where students lived for 5 days with local families as homestay guests.
Immersion in local culture and language took place concurrently with exploration of cloud forest
environments and introduction to tropical biodiversity and research methods.
The remainder of the program was spent at San Miguel Biological Station in the Cabo Blanco
Absolute Reserve. In San Miguel, workshops were held on taxonomy of tropical marine organisms,
and students were given hands-on instruction in the development of a research question;
fundamentals of experimental design and sampling; hypothesis testing, statistical analysis of data and
its interpretation; and writing up and presentation of research results. Students developed their own
research questions and carried out projects in small working groups, with oversight from program
faculty. Research reports were prepared and edited in consultation with faculty.
Small-group travel to additional sites of interest enabled students to carry out independent
explorations of the Arenal volcano, the Caribbean coast, and the Santa Elena area.
Initial findings were presented by the group in a research symposium. Formal presentation of these
research projects is an expectation of all participants, and may be done on each student’s home
campus, at undergraduate research symposia, at capstone festivals, and at conferences such as
SACNAS.
10
Details of Study Sites San Jose, the capital of Costa Rica, is located in the central highlands of the country at an elevation of
1150 m and has a moderate climate. The central valley is home to around half of the country’s
population of 4.75 million people.
Within the city are museums, markets, parks, plazas, cathedrals, restaurants, and the National
Theater. The group stayed at Hotel Cacts, a small bed-and-breakfast near Paseo Colon in downtown
San Jose.
San Luis de Monteverde is a rural community nestled at 1000-1200 m elevation below the continental
divide in the lee of the Tilarán Mountain Range. While in San Luis, each student lived with a host
family, sharing in the daily life of the family, and experiencing local culture and language first-hand.
The area is surrounded by tropical forest, plantings of coffee, bananas, vegetables, citrus, sugar cane,
and cattle pasture, and breathtakingly beautiful mountain scenery. The village borders the world-
famous Monteverde Cloud Forest Preserve, whose perpetual cover of dense, low clouds and mist gives
the Monteverde area its cloud forest vegetation. Weather varies from mild and sunny to damp and
chilly.
San Miguel Biological Station is located on the southern tip of the Nicoya Peninsula on the Pacific
coast, within Cabo Blanco Absolute Reserve, Costa Rica’s first national park. Because of its status as
an Absolute Reserve, the station has been closed to the general public since 1963, but welcomes a
limited number of student groups and researchers by special invitation. The climate is hot and
humid, with a mean temperature of 27 degrees C (81 degrees F). Annual rainfall is around 3 m, and is
highly seasonal in distribution; almost all the rain occurs between May-October.
The station has several important terrestrial and marine habitats, including tropical moist semi-
deciduous forest, coastal vegetation, permanent and seasonal streams, sandy beaches, extensive
tidepool formations, sheltered lagoons, wave-exposed beaches, and rocky headlands and reefs.
Snorkeling in the warm nearshore waters provides ready access to a diverse assemblage of tropical
reef fishes and invertebrates. San Miguel is reached by crossing the Gulf of Nicoya from Puntarenas
to Paquera by ferry, driving across the Nicoya Peninsula by bus, and hiking the last 2 kilometers into
the reserve.
Small groups traveled to three additional field sites for exploration of contrasting habitats. These
included Santa Elena de Monteverde, a cloud forest area with extensive ecotourism development; the
village of La Fortuna and Volcán Arenal, a large stratovolcano with recent lava flows in the Cordillera
de Tilaran; and Cahuita, a coastal site on the Caribbean known for its coral reef habitats.
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Maps
Map of Central America, showing location of Costa Rica between Nicaragua and Panama.
Map of Costa Rica. The three main study sites (San Jose, San Luis, and San Miguel) are shown with
filled circles; small group travel sites (Santa Elena, La Fortuna / Volcán Arenal, and Cahuita) are
shown with open circles .
12
Program Itinerary
ITINERARY, JUNE 10-JULY 25, 2012 / 46 DAYS
SUNDAY MONDAY TUESDAY WEDNESDAY THURSDAY FRIDAY SATURDAY
Jun 10
Final prep for
travel to San
Jose, Costa
Rica.
Overnight
flight.
Jun 11
Arrival Costa
Rica; welcome,
orientation.
Overnight San
Jose.
Jun 12
San Jose
Introductor
y lectures.
Overnight
San Jose.
Jun 13
San Jose
Intro
lectures,
homestay
preparation.
Overnight
San Jose.
Jun 14
Travel San
Jose to San
Luis, start
homestays.
Overnight
with host
families.
Jun 15
San Luis
Lectures,
orientation
session.
Overnight
with host
families.
Jun 16
San Luis
Lectures,
fieldwork in
cloud forest.
Overnight
with host
families.
Jun 17
San Luis
Lectures and
field activities.
Overnight with
host families.
Jun 18
San Luis
Cultural
activities.
Overnight with
host families.
Jun 19
Travel to
San Miguel
Biol.
Station,
Cabo Blanco
Jun 20
San Miguel.
Lectures,
fieldwork.
Overnight
San Miguel.
Jun 21
San Miguel.
Lectures,
fieldwork.
Overnight
San Miguel.
Jun 22
San Miguel.
Lectures,
fieldwork.
Overnight
San Miguel
Jun 23
San Miguel.
Lectures,
fieldwork.
Overnight
San Miguel
Jun 24
San Miguel.
Research
planning.
Overnight San
Miguel.
Jun 25
San Miguel.
Research.
Overnight San
Miguel.
Jun 26
San Miguel.
Research.
Overnight
San Miguel.
Jun 27
San Miguel.
Research.
Overnight
San Miguel.
Jun 28
San Miguel.
Research.
Overnight
San Miguel.
Jun 29
San Miguel,
Lectures,
Research.
Overnight
San Miguel.
Jun 30
San Miguel,
Lectures,
Research.
Overnight
San Miguel.
Jul 1
San Miguel,
Lectures,
Research.
Overnight San
Miguel.
Jul 2
San Miguel,
Lectures,
Research.
Overnight San
Miguel.
Jul 3
San Miguel,
Lectures,
Research.
Overnight
San Miguel.
Jul 4
San Miguel,
Lectures,
Research.
Overnight
San Miguel.
Jul 5
Depart for
small group
travel to
additional
field sites.
Jul 6
Small group
travel to
additional
field sites.
Jul 7
Small group
travel to
additional
field sites.
Jul 8
Small group
travel to
additional field
sites.
Jul 9
Return to San
Miguel, travel
debriefing..
Overnight San
Miguel.
Jul 10
San Miguel,
Lectures.
Research.
Overnight
San Miguel.
Jul 11
San Miguel.
Research,
analysis.
Overnight
San Miguel
Jul 12
San Miguel.
Research,
analysis.
Overnight
San Miguel
Jul 13
San Miguel.
Research,
writing.
Overnight
San Miguel
Jul 14
San Miguel.
Research,
writing.
Overnight
San Miguel
Jul 15
San Miguel.
Research,
analysis.
Overnight San
Miguel
Jul 16
San Miguel.
Research,
analysis.
Overnight San
Miguel
Jul 17
San Miguel.
Research,
writing.
Overnight
San Miguel
Jul 18
San Miguel.
Research,
writing.
Overnight
San Miguel
Jul 19
San Miguel.
Symposium
prep.
Overnight
San Miguel.
Jul 20
San Miguel.
Research
symposium.
Overnight
San Miguel.
Jul 21
San Miguel.
Research, ms.
editing.
Overnight
San Miguel.
Jul 22
San Miguel.
Final cleanup
and packing.
Overnight San
Miguel.
Jul 23
Travel to San
Jose. Ms.
editing.
Overnight San
Jose.
Jul 24
San Jose.
Final work,
banquet.
Overnight
San Jose
Jul 25
Program
evaluations.
Transfer to
airport.
Jul 26
Jul 27
Jul 28
13
Research Reports
14
Shell utilization by tropical hermit crabs under strongly contrasting levels of
protection and accessibility
ANTONIA ESTEVEZ-OLEA1, ALEJANDRO RIOS
2, ADRIENNE BLAYLOCK
3
& PHILLIP SCHOTTE4
1Department of Environmental Engineering, California Polytechnic State University, San Luis
Obispo, CA 93407 2 Department of Biology, California State University Monterey Bay, Seaside, CA 93955
3 Department of Biology, California State University East Bay, Oakland, CA 94542
4 Biosciences Department, Minnesota State University – Moorhead, Moorhead, MN 56563
ABSTRACT. Shell utilization was studied in the tropical terrestrial hermit crab, Coenobita
compressus, in two Pacific coastal sites in Costa Rica with strongly contrasting levels of
protection: San Miguel Biological Station, Cabo Blanco Absolute Reserve, which is closed to the
public, and Playa Carmen, Malpaís, which is one of Costa Rica’s most visited tourist beaches.
Hermit crabs were collected at random in replicate samples during the day and at night. Samples
of empty shells were randomly collected for reference at each site. Shells were identified to
species. Hermit crabs were weighed and an assessment was made of how well each crab fit its
shell.
The assemblage of empty shells included 51 species; hermit crabs were found to use 33
species. The total number of shell species, including both empty shells and shells used by hermit
crabs, was 62. The richness and diversity of empty shells was much higher in Cabo Blanco than
in Malpaís, although the diversity of shells used by hermit crabs was the same for the two sites.
Daytime samples of hermit crabs were more diverse than nighttime samples at each site, while
nighttime samples had larger crabs. Species composition of hermit crab shells differed between
sites and from day to night. There were substantial differences in species composition between
hermit crab samples and empty shells, indicating a high degree of selectivity on the part of the
crabs.
Nerita scabricosta shells were by far the most common species used by hermit crabs in
both locations and at both sampling times, although this species comprises only 0.5% of the
available empty shells. Malpaís crabs tended to be too large for the size of their shells, while
crabs from Cabo Blanco tended to fit their shells.
15
INTRODUCTION
The Cabo Blanco Absolute Reserve on the central Pacific coast of Costa Rica, Nicoya
Peninsula, Puntarenas Province, was the first protected area in the country, and the San Miguel
sector has been closed to the public since the reserve was formed in 1963. Human presence in
San Miguel de Cabo Blanco is strictly limited, and the area and its fauna since then have been
maintained in a pristine state, essentially undisturbed by human activity. Located 5 kilometers to
the north of the Reserve, Playa Carmen in the town of Malpaís is open to public access and is
one of Costa Rica’s most visited tourist beaches.
Terrestrial hermit crabs (Coenobita compressus: family Coenobitidae) are ubiquitous and
abundant on the shore and within the coastal vegetation on tropical Pacific shores. Hermit crabs
have soft, unprotected abdomens and occupy empty gastropod shells for protection against
predators, dessication, and osmotic stress (Shumway 1971, Hazlett 1981); they exchange these
for larger shells throughout their life as they grow.
Diversity of gastropods is very high along these shores, and many species of snail shells
are available for use by the hermit crabs. In this study, we investigated the assemblage of empty
shells available on the beach at each of the two study sites and compared it with the composition
and diversity of shells used by Coenobita compressus. We tested whether hermit crabs select
shells of some gastropod species over others, or if they take the shells that are most commonly
available. We assessed the weight distribution of hermit crabs and compared how well the crabs
fit their shells at the two sites.
The proximity of the pristine coastal habitat in San Miguel de Cabo Blanco to the
heavily-used beach at Playa Carmen in Malpaís provides a unique opportunity to compare
patterns of gastropod shell availability and hermit crab shell choice under strongly contrasting
levels of human disturbance, and to evaluate the effect of human activity on hermit crab
populations.
STUDY SPECIES
Worldwide, there are more than 800 species of hermit crabs (Crustacea, Order Decapoda,
Infraorder Anomura) (Hazlett 1981); of these, only the 12 species belonging to the family
Coenobitidae are terrestrial, inhabiting the dry areas above the tide line of tropical beaches
(Laidre 2010).
Lack of calcification of the abdominal skeleton requires hermit crabs to seek abandoned
snail shells (or other portable hollow objects) as shelter, and the combination of mobility and
protection provided by this life style may contribute to their great success; hermit crabs are
abundant in nearly all marine environments as well as on tropical terrestrial habitats (Hazlett
1981).
The abdomen of hermit crabs is asymmetrical, coiled in a spiral to conform to the shape
of gastropod shells, and the uropods or posterior appendages are modified as hooks for clinging
16
to the interior of the host shell (Debelius 2001). The muscular abdomen facilitates rapid
retraction into the shell (Jensen 1995).
The land hermit Coenobita compressus H. Milne Edwards 1837 ranges from Mexico to
Peru and westward across the Pacific to the shores of East Africa, and is found on protected or
semi-protected shores above the high tide level (Hickman & Zimmerman 2000). The chelipeds
or claws are unequal, with the left claw substantially larger; the claws are adapted for defense,
for holding large pieces of food, and for blocking the aperture of the shell when the crab
withdraws into the shell (Jensen 1995). Semi-enclosed gill chambers keep the gills moist,
enabling the animal to survive out of water (Hickman & Zimmerman 2000). The species has
been reported to be most active at night (Ball 1972), particularly during dry periods. Large
individuals are generally nocturnal, although smaller individuals tend to be more active during
the day (Abrams 1978).
The diet of hermit crabs is varied (Morris et al. 1980). Coenobita compressus in Cabo
Blanco can be seen scavenging on both plant material and dead animal matter; and when a food
source is located, large aggregations of hermit crabs quickly assemble to feed (personal
observation). Lindquist & Carroll (2004) document the impact of these crabs as predators of
seeds and young seedlings in the coastal forest of San Miguel de Cabo Blanco.
Almost all populations of hermit crabs occupy a wide range of shell types and sizes and
an extensive array of gastropod shell species; nonetheless, they tend to occupy a distinct subset
of the available species of gastropod shells (Hazlett 1981). The preferred shell type is generally
found to vary with the hermit crab species (Grant & Ulmer 1974, Mitchell 1976, Morris et al.
1980, Ricketts et al. 1985).
Shell availability is potentially a limiting resource for hermit crabs (Hazlett 1981). In
studies elsewhere, the growth rate and reproductive output of hermit crabs have been reported to
be influenced by the size and type of shell occupied (Bertness 1980). Hermit crabs in tightly-
fitting shells do not grow as rapidly as those with shells that fit well, and are more susceptible to
predation if they are unable to retract completely into the shell (Angel 2000). Shell availability
has been shown to limit the abundance of hermit crabs (Kellogg 1976).
METHODS
The location of the two sampling sites is shown in Figure 1. San Miguel Biological
Station in the western sector of the Cabo Blanco Absolute Reserve is located at the southern tip
of the Nicoya Peninsula, Puntarenas Province, Costa Rica (9o34’42” N, 85
o08’08” W). Playa
Carmen is located in the town of Malpaís, 5 kilometers to the north of the Reserve (9o37’32” N,
85o09’04” W).
Sampling was done between 23-28 June 2012. Empty gastropod shells were collected
from each site during daytime low tides; live hermit crabs were collected from each site at low
tides both during the day and at night.
17
Assemblage of empty shells. Replicate sample bags with 15 empty gastropod shells each
were collected from Cabo Blanco (77 bags) and Malpaís (70 bags). A random numbers table
was used to determine the starting point for each sample; collection began when the first empty
shell was located and gathered, followed by the next 14 shells to be encountered. Shells from the
sample bags were identified to species.
The assemblage of empty shells collected in this manner was used as a null model of
available shell diversity and composition.
Live hermit crab samples. Replicate sample bags with 15 live hermit crabs in each were
collected at each of the two sampling sites (Cabo Blanco, Malpaís) during each of the two
sampling periods (daytime, nighttime). A random numbers table was used to determine the
starting point for each sample. Collection began when the first hermit crab was located and
gathered, followed by the next 14 to be encountered.
A total of 35 sample bags were collected at each site during each sampling time. The
shell of each hermit crab was identified to species. Weight (precision 0.1 g) was determined for
a random subsample of hermit crabs from each site and from each sampling time; the total
weight of the crab plus its shell was recorded. Shell fit was scored for each hermit crab
according to the following categories: loosely-fitting (having ample room for growth); tightly-
fitting (unable to retract the body inside the shell), or fitting well in the shell. Following
identification and measurement in the laboratory, the hermit crabs were released.
Hermit crab identification follows Mena Aguilar (1995). Taxonomy of shells is based on
Keen (1971), updated with information from the World Register of Marine Species WoRMS
(Appeltans et al. 2012).
RESULTS
Species accumulation curves for empty gastropod shells (Figure 2) were prepared for the two
sites using replicate samples of 15 shells each. The total species richness of shells for Cabo
Blanco samples (77 replicate samples, 1155 shells) was 50, and that for Malpaís (70 replicate
samples, 1050 shells) was 31. The curve for the Cabo Blanco empty shell assemblage was still
increasing, and more extensive sampling would likely yield more species of empty shells; thus
50 species is an underestimate of the true species richness. In contrast, the curve for the Malpaís
assemblage appears to have leveled off, indicating that sampling was adequate to reflect species
richness. When empty shell samples from both sites are pooled, the total number of shell species
represented is 51.
Species accumulation curves for shells of live hermit crabs (Figure 3) were prepared for
daytime and nighttime samples from each of the two sites. Each curve was based on 35 replicate
samples of 15 live crabs each (525 individuals). The species richness of shells for hermit crabs
in Cabo Blanco was 19 (daytime) and 23 (nighttime); that in Malpaís was 25 (daytime) and 23
(nighttime). The accumulation curves for live crabs appear to have leveled off in all four cases,
indicating that sample sizes are adequate for estimates of richness.
18
Table 1 summarizes species richness for the various samples and combinations of
samples. In Cabo Blanco, the total assemblage of empty shells plus shells used by hermit crabs
was 59 species; combining daytime and nighttime samples, crabs in Cabo Blanco made use of 25
out of the 59 species available, or 42% of the available pool, and rejected the remaining 58% of
species. In Malpaís, the total assemblage of empty shells plus those found on hermit crabs was
45 species; taking daytime and nighttime samples together, crabs in Malpaís used 30 out of the
45 species available, or 67% of the species pool, and rejected the remaining 33%.
When hermit crabs from the four groups of samples are pooled, the total number of shell
species used is 33. The total assemblage, taking into account all samples of empty shells and
hermit crabs in the study, was 62 shell species; thus crabs in the study area as a whole made use
of 53% of the total species available, and rejected the remaining 47%.
Shell species composition is shown in Figure 4 for empty shell samples from Cabo
Blanco and Malpaís. Composition of the empty shell assemblage was generally similar between
the two sites, although the number of species was far greater in Cabo Blanco. In both sites, the
most abundant species was the olive shell Oliva spicata, which made up 50% of empty shells
from Cabo Blanco and 65% of empty shells from Malpaís. Other species of empty shells found
commonly at both sites were the keyhole limpet Fissurella macrotrema and the cone shell Conus
perplexus.
Species composition of shells occupied by live hermit crabs is shown in Figure 5;
composition is shown for both sites at both sampling times. In all four cases, the predominant
species was the tooth shell Nerita scabricosta, which in Cabo Blanco made up 47% of
individuals by day and 57% by night (52% overall for Cabo Blanco), and in Malpaís made up
29% of individuals by day and 51% by night (40% overall for Malpaís). Combining all samples,
tooth shells were used by 46% of hermit crabs collected in this study. In contrast, empty tooth
shells were almost never encountered on the beach; in Cabo Blanco, this species represented
0.7% of empty shells sampled, and in Malpaís 0.4% of empty shells. Considering both sites,
tooth shells made up only 0.5% of the empty shells sampled.
Other species commonly used by hermit crabs in the four samples were the rock shell
Acanthais brevidentata, (8% of individuals overall), the whelk Cantharis panamicus (7%), the
rock shell Thais melones (6%), the rock shell Neorapana muricata (5%), the planaxid Planaxis
planicostatus (4%), the turban shell Turbo saxosus (4%), and the cerith Cerithium nicaraguense
(4%).
A detailed record of shell species distributions among empty shells and hermit crab
samples is given in Appendix 1.
A total of 32 gastropod families were encountered when all samples (both empty shells
and hermit crabs) are considered (Figure 6). Among the samples of empty shells, 27 families
were represented. The most common empty shells were Olividae (olive shells), which made up
58% of the individuals; Conidae (cone shells), 13%; Fissurellidae (keyhole limpets), 8%;
Muricidae (rock shells), 7%; and Columbellidae (dove shells), 4%.
19
Among the samples of hermit crabs, 21 shell families were found. The most abundant
were Neritidae (tooth shells), accounting for 46% of the total; Muricidae (rock shells), 24%;
Buccinidae (whelks), 8%; Cerithiidae (ceriths), 7%; Planaxidae (planaxids), 4%; and Turbinidae
(turban shells), 4%. As seen in Figure 6, the composition differs dramatically between empty
shells and hermit crabs; the assemblage of shell families used by hermit crabs in this area bears
little resemblance to the available pool of empty shells.
A detailed record of shell families found among empty shells and hermit crab samples is
presented in Appendix 2.
Species composition of samples was analyzed using DCA, or detrended correspondence
analysis, using PCORD 6 software (McCune & Mefford 2011). DCA ordinates samples based
on species composition, and reciprocally ordinates species based upon the samples in which they
are found. Quantitative data (number of individuals per species) were used. An ordination of
all 287 samples and 62 species (Figure 7) produced a complete separation of empty shell samples
and live crab samples on the first ordination axis.
A subsequent ordination of samples of empty shells alone (Figure 8) suggests an apparent
difference in species composition between Cabo Blanco and Malpaís samples. Axis 1 scores
from the two sites were compared using a Kolmogorov-Smirnov two-sample test, and were
found to differ (Dmax= 0.730, n1= 70, n2=77; P<0.001).
An ordination of all live samples was carried out (Figure 9), and the results on the first
axis suggest differences among the two sites and the two sampling times. Axis 1 values for these
four groups were compared using a Kolmogorov-Smirnov two-sample tests. Differences were
found between Cabo Blanco day and night samples (Dmax= 0.609, n1= 35, n2=35; P<0.001);
Malpaís day and night samples (Dmax= 0.715, n1= 35, n2=35; P<0.001); Cabo Blanco and
Malpaís daytime samples (Dmax= 0.486, n1= 35, n2=35; P<0.001); and Cabo Blanco and
Malpaís nighttime samples (Dmax= 0.598, n1=35, n2=35; P<0.001).
Shannon’s diversity H’ was calculated for all samples (Table 1); H’ values were
compared using a special formulation of the t-test (Hutcheson 1970). Shannon’s diversity for
empty shells was greater in Cabo Blanco (H’=2.075) than in Malpaís (H’=1.468) (t=8.178, 178
d.f.; P<0.001). Among hermit crabs, the diversity of Cabo Blanco samples (H’=1.977) did not
differ from that of Malpaís samples (H’= 2.077).
Empty shells from Cabo Blanco did not differ in species diversity from shells of hermit
crabs at that site; however in Malpaís, samples of empty shells were less diverse than samples of
hermit crabs (t=8.646, 2008 d.f; P<0.05).
Shell diversity values were compared for samples of crabs collected by day and night.
Within Cabo Blanco, daytime samples (H’=2.030) had higher shell diversity than nighttime
samples (H’=1.823) (t=2.356, 1042 d.f.; P<0.05). Likewise, in Malpaís, shells of daytime
samples (H’=2.101) were more diverse than those of nighttime samples (H’=1.826) (t=3.623,
940 d.f.; P<0.001).
20
Daytime samples from Cabo Blanco did not differ in diversity from daytime samples
from Malpaís, nor did nighttime samples differ in diversity between the two sites.
Pielou’s evenness J was calculated for all samples (Table 1). Among samples of empty
shells, evenness was higher in Cabo Blanco than in Malpaís, although both sites were dominated
by Oliva spicata shells. Among hermit crabs, evenness during the day was higher in Malpaís
than in Cabo Blanco, although nighttime values were comparable. At each sites, evenness was
higher during the day than at night. The assemblage of empty shells had consistently lower
evenness than that of the hermit crab samples.
Weight distributions were determined for hermit crabs collected from the two sites during
daytime and nighttime sampling (Figure 10). Pairwise comparisons using a Kolmogorov-
Smirnov two-sample test show that crab weights at each site were lower during the day than at
night. During the day, crab weights did not differ between the two sites (Cabo Blanco
mean=0.82 g, Malpaís mean 1.20 g); however at night, crabs from Cabo Blanco (mean=6.20 g)
weighed less than those from Malpaís (mean=8.23 g).
Shell fit was scored for hermit crabs collected at the two sites and during the two
sampling times. Each crab was scored as having shell that fit loosely, fit well, or fit tightly; for
purposes of analysis, the first two categories (fitting loosely or fitting well) were combined, and
were considered to represent a good fit. Contingency table analyses were used to test for
association between shell fit (good vs. tight) and site (Cabo Blanco vs. Malpaís). Tests were
done separately for daytime and nighttime samples. For samples collected during the day, shell
fit was independent of location (Table 2; G=0.794, 1 d.f.; P >0.05). At night, however, tightly-
fitting shells were most often found in Malpaís, while shells of Cabo Blanco hermit crabs tended
to fit well (Table 3; G=437.692, 1 d.f.; P<0.001).
Contingency tables were also used to test for association between shell fit and time of
sampling; tests were done separately for the two sites. In neither location was shell fit
independent of time of day. In Cabo Blanco, tightly-fitting shells tended to be found during the
day (Table 4; G=17.562, 1 d.f.; P<0.001); in Malpaís, tightly-fitting shells tended to be found at
night (Table yy; G=15.232, 1 d.f.; P<0.001).
DISCUSSION
Hermit crabs in this study are clearly highly selective in their choice of shells. Species
composition and family makeup of empty shells and those used by hermit crabs were remarkably
distinct from one another.
There is no clear consensus on certain key aspects of hermit crab shell choice. In a global
survey of hermit crab shell use, Barnes (2003) found the number of shell types to vary with the
genus of hermit crab; crabs of the genera Coenobita, Clibanarius and Calcinus used more types
of shells than did those of Dardanus, Diogenes, and Pagurus. In his study, the number of shell
species used among the various hermit crab populations studied ranged from 3-18 among two
subtidal hermit crab genera. More shell species were used among tropical populations than
among temperate populations of hermit crabs, mirroring the trend in diversity of live gastropods.
21
Hazlett (1981), in contrast, reported the number of shell species occupied by hermit crab
populations to range from 4-34, and found no latitudinal trends in diversity of shell species.
The hermit crabs in our samples made use of 33 shell species in 21 families, which is
close to the maximum cited by Hazlett. The 33 species represents 53% of the total pool
available; 29 species were rejected. Our two study sites differed in the number of shell species
used as well as the number rejected: in Cabo Blanco, crabs used 25 species (42% of the
available pool) and rejected 34, while in Malpaís, crabs used 30 species (67% of the pool) and
rejected only 15.
The null assemblage in this study was generated by collecting shells randomly from the
beach. Hermit crabs not only pick up empty shells from the beach, but also take shells from
other hermit crabs. Abrams (1976) found that Coenobita preferred shells which had been
previously used by other individuals of Coenobita; this preference arises because of shell
modification by the hermit crabs, which increases the effective interior volume of the shell.
Because shells are so often recycled from one hermit crab to another, one significant component
of the pool of available shells would be the set of shells currently in use by the hermit crabs
themselves. The degree of wear on hermit crab shells was seen to vary markedly from one
individual to the next in our samples, although we did not score this in our assessments. An
estimate of shell wear would be of interest in future studies, allowing a comparison of the degree
of recycling experienced by shells in different sites.
In a study of shell selection and utilization by Coenobita compressus in southern Costa
Rica and Panama, Abrams (1978) noted that the tooth shell Nerita scabricosta was most
commonly used, making up 40.6% of the sample, and was preferred over other shell species.
The predominance of Nerita scabricosta mirrors the results of an earlier survey in San Miguel
(Pourtaverdi & Schotte 2011), and is in keeping with our current findings: at both sites and
during both sampling times, tooth shells were the most frequently used, accounting for 46% of
all hermit crab shells overall. Among empty shells collected from the beach, tooth shells make
up a mere 0.5% of the assemblage.
Tooth shells have several features that may contribute to their popularity among hermit
crabs. Their large, round aperture and roomy body whorl (Figure 11) provides ready access to
the shell and ample room for growth. In a comparative study of the biomechanics of hermit
crabs and their shells in Cabo Blanco, Nowacki et al. (2012) reported that tooth shells were
highly resistant to crushing, and that hermit crabs using tooth shells performed as well or better
than others in trials of speed and pulling strength.
The ultimate source of empty shells available for use by hermit crabs is the community of
living gastropods. Nerita scabricosta snails are extremely abundant in the study area. In a
survey of gastropod species composition in the rocky intertidal habitats of the San Miguel sector
of Cabo Blanco, tooth shells were found to comprise 60% of all live snails (Hamilton et al.
2011).
22
Tooth shells, known locally in Spanish as burgados, are a delicacy, and wherever permitted
they are gathered for food. Tooth shells may be prepared as ceviche, marinated in lime juice
with cilantro and minced sweet peppers, or cooked with rice and served as arroz con burgados, a
traditional dish at wedding feasts. Snails measuring ≥ 1.0-1.5 cm are taken (L.Gomez Gomez,
pers. comm.). The San Miguel populations of tooth shells, within Cabo Blanco Absolute
Reserve, are strictly protected from harvesting. A comparative study of Nerita populations
inside and outside the reserve (Retana et al. 2012) found the largest individuals to be present in
Cabo Blanco; large snails were fewest where the public has unlimited access, and were
intermediate in density where limited collecting is allowed. When live Nerita snails are gathered
for food, the empty shells are not as a rule returned to the shore. Hence exploitation of tooth
shells by humans may affect availability of this species for hermit crabs outside the reserve.
Due to strictly controlled access and limited human impact, shells within the San Miguel
sector of Cabo Blanco are left in place and are not taken from the reserve. Visitors to public
beaches such as Playa Carmen in Malpaís typically collect shells as souvenirs. Shells picked up
by tourists are unlikely to be a random sample, but should tend to favor the largest and most
intact shells encountered. Further, Playa Carmen artisans and street vendors enjoy a thriving
trade in hand-crafted jewelry made from shells gathered on the beach. Human activity in the
Malpaís area could potentially contribute to a decrease in species diversity, loss of preferred
species, and reduction in size ranges of shells available to hermit crabs.
Shell composition, diversity and size may be limiting to hermit crabs in Malpaís. The
species composition of empty shells differed from that in Cabo Blanco, despite the proximity of
the two sites. The species richness, family richness, and diversity of empty shells was lower
there than in Cabo Blanco. Availability of tooth shells, the preferred species, was lower, and the
proportion of hermit crabs using tooth shells was substantially less.
Finally, hermit crabs in Malpaís tended to have more tightly-fitting shells, especially at
night, suggesting that suboptimal shells were retained and worn longer than was seen in Cabo
Blanco. Use of tightly-fitting shells has been shown in other studies to bring about slower
growth rates and increased risk of predation (Angel 2000). Crabs unable to retract into the shell
may be at risk of desiccation as well; however, further research is needed to test whether this
explains the prevalence of nocturnal activity in crabs with tightly-fitting shells.
The density of hermit crabs was not quantified in the two sites, and so a rigorous
comparison of crab abundance is not possible. Based on the amount of time necessary to
complete the sampling, it appears that hermit crabs were extremely abundant at night at both
sites and during the day in Cabo Blanco, but were substantially less so during the day in Malpaís.
This impression awaits confirmation based on quantitative data.
ACKNOWLEDGEMENTS
Diana Lieberman assisted with shell identification, experimental design, and editing of
the manuscript. Data analysis made use of software written by Milton Lieberman. Support for
this research was provided by the Chancellor´s Office of the California State University and NSF
grant HRD-0802628. Programmatic funding came from CSU-Monterey Bay’s SEP.org.
23
LITERATURE CITED
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compressus (H. Milne Edwards). Oecologia 34: 239-253.
ANGEL, J.E. 2000. Effects of shell fit on the biology of the hermit crab Pagurus longicarpus
(Say). Journal of Experimental Marine Biology and Ecology 243: 169-184.
APPELTANS W., BOUCHET, P., BOXSHALL, G.A., DE BROYER, C., DE VOOGD, N.J.,
GORDON, D.P., HOEKSEMA, B.W., HORTON, T., KENNEDY, M., MEES, J., POORE,
G.C.B., READ, G., STÖHR, S., WALTER, T.C. & COSTELLO, M.J. (eds). 2012. World
Register of Marine Species. Accessed at http://www.marinespecies.org on 2012-10-02.
BALL, E.E. 1972. Observations on the biology of the hermit crab Coenobita compressus H.
Milne Edwards (Decapoda; Anomura) on the west coast of the Americas. Revista de Biologia
Tropical 20: 265-273.
BARNES, D.K.A. 2003. Local, regional and global patterns of resource use in ecology: hermit
crabs and gastropod shells as an example. Marine Ecology Progress Series 246: 211-223.
BERTNESS, M.D. 1980. Shell preference and utilization patterns in littoral hermit crabs of the
bay of Panama. Journal of Experimental Marine Biology and Ecology 48: 1-16.
DEBELIUS, H. 2001. Crustacea guide of the world. IKAN-Unterwasserarchiv, Frankfurt,
Germany.
GRANT, W.C. & ULMER, K.M. 1974. Shell selection and aggressive behavior in two
sympatric species of hermit crabs. Biological Bulletin 146: 32-43.
HAMILTON, J., WOLF, M. & SANTOS, B.A. 2011. Diversity and distribution of marine
gastropod species along the upper intertidal zone of Playa San Miguel, Cabo Blanco Absolute
Reserve, Costa Rica. Pp. 20-34 in Lieberman, D. & Leiker, S. (eds.), Expedition Report, CSU-
LSAMP Costa Rica Research Program, Summer 2011. California State University Monterey
Bay, Seaside, CA.
HAZLETT, B.A. 1981. The behavioral ecology of hermit crabs. Annual Review of Ecology and
Systematics 12: 1-22.
HICKMAN, C.P. & ZIMMERMAN, T.L. 2000. A field guide to crustaceans of Galápagos.
Sugar Spring Press, Lexington, VA.
HUTCHESON, K. 1970. A test for comparing diversities based on the Shannon formula.
Journal of Theoretical Biology 29: 151-155.
JENSEN, G.C. 1995. Pacific coast crabs and shrimps. Sea Challengers, Monterey, CA.
24
KEEN, M.A. 1971. Sea shells of tropical west America. 2nd edition. Stanford University Press,
Stanford, California.
KELLOGG, C.W. 1976. Gastropod shells: a potentially limiting resource for hermit crabs.
Journal of Experimental Marine Biology and Ecology 22: 101-111.
LAIDRE, M.E. 2010. How rugged individualists enable one another to find food and shelter:
field experiments with tropical hermit crabs. Proceedings of the Royal Society B 277: 1361-
1369.
LINDQUIST, E.S. & CARROLL, C.R. 2004. Differential seed and seedling predation by crabs:
impacts on tropical coastal forest composition. Oecologia 141: 661-671.
MCCUNE, B. & MEFFORD, M.J. 2011. PC-ORD. Multivariate Analysis of Ecological Data.
Version 6. MjM Software, Gleneden Beach, OR.
MENA AGUILAR, L.A. 1995. Inventario de invertebrados de la zona de entremareas de la
Reserva Natural Absoluta de Cabo Blanco, Peninsula de Nicoya, Costa Rica. Ministerio de
Recursos Naturales, Energia y Minas (MIRENEM), Reserva Natural Absoluta Cabo Blanco,
Costa Rica.
MITCHELL, K.A. 1976. Shell selection in the hermit crab Pagurus bernhardus. Marine
Biology 35: 335-343.
MORRIS, R.H., ABBOTT, D.P. & HADERLIE, E.C. 1980. Intertidal invertebrates of
California. Stanford University Press, Stanford, CA.
NOWACKI, A., HERNANDEZ, A. & DE LA PARRA, J.C. 2012. Comparison of
biomechanical properties of hermit crabs using contrasting shell types on a tropical shore. Pp.
108-131 in Lieberman, D. & Leiker, S. (eds.), Expedition Report: CSU-LSAMP Costa Rica
Research Program, Summer 2012. California State University Monterey Bay, Seaside, CA.
POURTAVERDI, J. & SCHOTTE, P. 2011. Hermit crab shell choice on a pristine tropical
beach at Cabo Blanco Absolute Reserve, Costa Rica. Pp. 72-85 in Lieberman, D. & Leiker, S.
(eds.), Expedition Report, CSU-LSAMP Costa Rica Research Program, Summer 2011.
California State University Monterey Bay, Seaside, CA.
RETANA, J., ESCOBAR, E. & FRANCO, D. 2012. Comparison of protected and exploited
tooth shell populations (Nerita scabricosta) on the Pacific coast of Costa Rica. (In preparation).
RICKETTS, E.F., CALVIN, J. & HEDGPETH, J.W. 1985. Between Pacific tides. 5th edition.
Revised by D.W. Phillips. Stanford University Press, Stanford, CA.
SHUMWAY, S.E. 1978. Osmotic balance and respiration in the hermit crab, Pagurus
bernhardus, exposed to fluctuating salinities. Journal of the Marine Biological Association of
the U.K. 58: 869-76.
25
Table 1. Species richness, diversity, evenness, and family richness of assemblages of (a) empty
gastropod shells and (b) shells used by live hermit crabs. Samples were taken from Cabo Blanco
and Malpaís; live hermit crabs at each site were sampled during daytime and nighttime low tides.
Species Shannon's Pielou's Number
Sample richness diversity evenness of
size s H' J families
(a) Empty shells
Cabo Blanco 1155 50 2.075 0.530 27
Malpaís 1050 31 1.468 0.424 19
Both sites pooled, empty shells 2205 51 1.869 0.453 27
(b) Hermit crabs
Cabo Blanco
Day 525 19 2.030 0.689 13
Night 525 23 1.823 0.581 13
Cabo Blanco, crab samples pooled 1050 25 1.977 0.614 14
Cabo Blanco, empty shells and crabs
pooled 2205 59
Malpaís
Day 525 25 2.101 0.758 16
Night 525 23 1.826 0.582 14
Malpaís, crab samples pooled 1050 30 2.077 0.611 19
Malpaís, empty shells and crab samples
pooled 2100 45
Both sites pooled, hermit crabs 2100 33 2.152 0.616 21
All samples, empty shells and crabs pooled 4305 62 2.152 0.616 21
Table 2. Test for association between shell fit and sample site (daytime samples only). Shell fit
was independent of location during the day; the proportion of individuals with tightly-fitting
shells was similar at the two sites (G=0.794, 1.d.f.; P>0.05).
Shell fit
Total Good Tight
Cabo Blanco 402 120 522
Malpaís 419 142 561
Total 821 262 1083
26
Table 3. Test for association between shell fit and sample site (nighttime samples only).
Tightly-fitting shells tended to be found in Malpaís samples (G=437.692, 1 d.f.; P<0.001).
Shell fit
Total Good Tight
Cabo Blanco 463 70 533
Malpaís 133 389 522
Total 596 459 1055
Table 4. Test for association between shell fit and time of day (Cabo Blanco samples only). In
Cabo Blanco, tightly-fitting shells were more often found during the day (G=17.562, 1 d.f.;
P<0.001).
Shell fit
Total Good Tight
Day 402 120 522
Night 463 70 533
Total 865 190 1055
Table 5. Test for association between shell fit and time of day (Malpaís samples only). In
Malpaís, tightly-fitting shells were most often found at night (G=15.232, 1 d.f.; P<0.001).
Shell fit
Total Good Tight
Day 419 142 561
Night 133 389 522
Total 552 531 1083
27
8 km
Figure 1. Map of study area showing location of the two sample sites. Playa Carmen in Malpaís
is a popular tourist resort; San Miguel within the Cabo Blanco Absolute Reserve is closed to the
public. The two sites are separated by approximately 5 km. Inset map: southern tip of the
Nicoya Peninsula, Puntarenas Province, Costa Rica.
28
Figure 2. Species accumulation curves for samples of empty gastropod shells collected from
Cabo Blanco and Malpaís. Each replicate sample contains 15 shells. The Cabo Blanco samples
(circles) include 77 replicate samples with 1155 individual shells; those for Malpaís (diamonds)
include 70 samples with 1050 shells.
Figure 3. Species accumulation curves for samples of live hermit crabs collected from Cabo
Blanco and Malpaís; samples at each site were taken both during the day and at night. Each
curve is based on 35 replicate samples of 15 crabs each (525 individuals). Circles, Cabo Blanco;
diamonds, Malpaís. Open symbols, daytime samples; closed symbols, nighttime samples.
0
10
20
30
40
50
60
70
80
0 10 20 30 40 50 60 70 80
Nu
mb
er o
f sp
ecie
s
Number of samples (15 empty shells per sample)
0
10
20
30
40
50
0 10 20 30 40 50 60 70 80
Nu
mb
er o
f sp
ecie
s
Number of samples (15 hermit crabs pers sample)
29
Figure 4. Number of individuals of each species in samples of empty shells collected from (a)
Cabo Blanco (total 51 species) and (b) Malpaís (total 31 species). Species are ordered by rank of
abundance. Names are abbreviated by the first three letters of the genus and the first one or two
letters of the species. Oliva spicata (Olis) is the most common species in both sites.
30
0
100
200
300
400
500
600
700
Ner
sA
cab
Pla
pC
ern
Co
np
Tegp
Thas
Neo
mTh
amA
nab
Can
pEc
ha
Co
lfSt
ylB
ulp
Turs
Plip
Leu
cB
urc
Freq
uen
cy
Shell species
0
100
200
300
400
500
600
700
Ner
sTh
amA
cab
Pla
pTu
rsC
ern
Neo
mC
anp
Tegp
Cer
mTh
asB
urc
Cer
gLe
uc
An
abG
ems
Co
lfM
alr
Cer
aB
ulp
Cym
tC
olm
Ech
a
Freq
uen
cy
Shell species
31
Figure 5. Number of individuals of each shell species in samples of live hermit crabs collected
from (a) Cabo Blanco, daytime (total 19 species), (b) Cabo Blanco, nighttime (total 23 species),
(c) Malpaís, daytime (total 25 species), and (d) Malpaís, nighttime (total 23 species). Species are
ordered by rank of abundance. Names are abbreviated by the first three letters of the genus and
the first one or two letters of the species. Nerita scabricosta (Ners) is the most common species
in all four groups.
0
100
200
300
400
500
600
700
Ner
s
Aca
b
Can
p
Neo
m
Cym
t
Tham
Cer
m
Thas
Tecp
Turs
Cer
n
Pla
p
Gem
s
Bu
rc
An
ab
Serm
Jen
p
Leu
c
Co
lf
Bu
lp
Turl
Fism
Uva
b
Mit
l
Po
lt
Freq
uen
cy
Shell species
0
100
200
300
400
500
600
700
Ner
sC
anp
Tham Tu
rsA
cab
Neo
mC
ymt
Pla
pB
urc
Thas
Tegp
Mal
rG
ems
Cer
mLe
uc
Op
epA
nab
Cer
nP
olt
Mo
nv
Har
cC
erg
Mit
l
Freq
uen
cy
Shell species
32
Figure 6. Number of individuals in each shell family from samples of (a) live hermit crabs (total
2136 individuals, 21 families) and (b) empty gastropod shells (total 2052 individuals, 27
families). Data from Cabo Blanco and Malpaís are pooled, as are daytime and nighttime
samples. Families are ordered alphabetically.
0
100
200
300
400
500
600
700
800
900
1000
Freq
uen
cy
(a) Live crabs
0
100
200
300
400
500
600
700
800
900
1000
1100
1200
Arc
hit
ecto
nic
idae
Bu
ccin
idae
Bu
llid
ae
Bu
rsid
ae
Cal
yptr
ae
Can
cella
r
Cer
ith
iidae
Co
lum
bel
lidae
Co
nid
ae
Cym
atiid
ae
Cyp
raei
dae
Fasc
iola
riid
ae
Fiss
ure
llid
ae
Har
pid
ae
Litt
ori
nid
ae
Mit
rid
ae
Mu
rici
dae
Nas
sari
idae
Nat
icid
ae
Ner
itid
ae
Oliv
idae
Ped
icu
lari
idae
Pla
nax
idae
Pu
lmo
nat
a
Sip
ho
nar
iidae
Ton
nid
ae
Triv
iidae
Tro
chid
ae
Turb
inid
ae
Turr
itel
lidae
Ver
met
idae
Vo
luti
dae
Freq
uen
cy
Family
(b) Empty shells
33
Figure 7. Ordination of samples of live hermit crabs from Cabo Blanco (c) and Malpaís (m) and
samples of empty gastropod shells (e) from both sites. There is a complete separation on axis 1
between hermit crab samples and empty shell samples, indicating a marked difference in species
composition between the two.
Axis 1
Axi
s 3
34
Figure 8. Ordination of samples of empty gastropod shells collected from Cabo Blanco (c) or
Malpais (m). Although there is appreciable overlap, differences in axis 1 values, and hence in
species composition, were found between the two sites.
Axi
s 2
Axis 1
35
Figure 9. Ordination of samples of live hermit crabs collected from Cabo Blanco during daytime
(c) and nighttime (cn) sampling times, and from Malpaís during daytime (m) and nighttime (mn)
sampling times. Although there is appreciable overlap, differences in axis 1 values, and hence in
species composition, were found between the two sampling times for each site (Cabo Blanco day
vs. night; Malpaís day vs. night) and between the two sites (Cabo Blanco vs. Malpaís, day; Cabo
Blanco vs. Malpaís, night).
Axis 1
Axi
s 2
36
0
40
80
120
160
200
240
280
320
360
1 6 11 16 21 26 31 36
Nu
mb
er o
f in
div
idu
als
Weight (g)
(a) Cabo Blanco, day
0
40
80
120
160
200
240
280
320
360
1 6 11 16 21 26 31 36
Nu
mb
er o
f in
div
idu
als
Weight (g)
(b) Cabo Blanco, night
37
Figure 10. Weight distributions for samples of hermit crabs collected from Cabo Blanco and
Malpaís during daytime and nighttime sampling. (a) Cabo Blanco, day; (b) Cabo Blanco, night;
(c) Malpaís, day; (d) Malpaís, night. Weight includes both the crab and its shell. At each site,
crabs sampled at night weighed more than those sampled during the day.
0
40
80
120
160
200
240
280
320
360
1 6 11 16 21 26 31 36
Nu
mb
er o
f in
div
idu
als
Weight (g)
(c) Malpaís, day
0
40
80
120
160
200
240
280
320
360
1 6 11 16 21 26 31 36
Nu
mb
er o
f in
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idu
als
Weight (g)
(d) Malpaís, night
38
Figure 11. Empty shell of the tooth shell Nerita scabricosta, showing the large, round aperture
and roomy body whorl. Tooth shells were the predominant species used by hermit crabs at both
Cabo Blanco and Malpaís. (Photograph courtesy of J. Retana).
39
40
41
42
Analysis of sediments carried by a tropical intertidal sea cucumber,
Holothuria inornata, on the Pacific coast of Costa Rica
MARK JACKSON1, KARA NYGAARD
2 & ARELI TEJEDA
3
1 Wildlife Biology Program, University of Montana, Missoula, MT 59812
2 Department of Biosciences, Minnesota State University – Moorhead, Moorhead, MN 56563
3 Biology Program, California State University Channel Islands, Camarillo, CA 93012
ABSTRACT. The sea cucumber Holothuria inornata is typically found coated with sediments and
particulate debris from its surroundings. A total of 30 sea cucumbers were collected from the
intertidal zone at Cabo Blanco Absolute Reserve on the Pacific coast of Costa Rica, and the
sediments adhering to them were removed for analysis.
Sea cucumbers ranged in length from 94-193 mm. The total dry weight of sediments
carried ranged from 1.3 – 23.7 g (mean 9.4 g); sediment load was independent of the size of the
sea cucumber. The mean composition of sediments was 45% shell, 30% pebble, and 25% sand,
with substantial variation in composition from one individual to another. Sediment composition
was similar over all three body regions of the sea cucumbers (head, median, and posterior).
The percent cover of substrate types in the field, based on point sampling within the sea
cucumber habitat, were 38% pebble, 38% sand, and 24% sand, which is quite distinct from the
composition borne by sea cucumbers. This study indicates that sea cucumbers are selective in
their use of substrate materials, and do not randomly acquire sediments in proportion to their
availability.
INTRODUCTION
Sea cucumbers (Echinodermata: Holothuroidea) are an important component of the
intertidal and shallow water fauna on tropical shores. These elongate, cylindrical, limbless
invertebrates feed on sediment from which they extract organic materials.
Known predators of sea cucumbers include lobsters, turtles, and fish large enough to
swallow sea cucumbers whole (Hickman 1998). Sea cucumbers have a number of behavioral
and structural adaptations which serve to protect them from predation. Nearly all sea cucumbers
have a potent toxin in the body wall which shows significant toxicity to fish and other predators
(Hyman 1955, Hickman 1998). Cuvierian tubules are present in many sea cucumbers; these
sticky white threads are ejected violently through the anus and entangle and immobilize
43
predators such as small fish (VandenSpiegel & Jangoux 1987, VandenSpiegel, Jangoux &
Flammang 2000). Evisceration, in which the internal organs of the sea cucumber are suddenly
expelled with great force, occurs as a response to stress or attack, and may temporarily distract a
predator; the lost viscera are later regenerated (Hyman 1955, Mosher 1956).
A few species of sea cucumbers cover the exposed surfaces of their bodies with an
accumulation of sediments or debris which they obtain from their surroundings. The function of
this behavior is not known. The coating of sediments could act as visual or chemical
camouflage, or could protect the skin from bites; alternatively, the coating of sediments could
protect the skin from solar radiation or insulate the animal from heat. While there is no shortage
of plausible hypotheses, rigorous evidence that would point toward one explanation over another
is lacking.
Further, the most basic quantitative information on the types and amounts of sediments
collected by sea cucumbers remains unknown. Such fundamental information, while of interest
in its own right, might also shed light on the significance of this poorly-understood behavior.
The study species, Holothuria inornata, characteristically covers the exposed areas of its
back with a variety of sediments and particulate matter. The species is commonly found in rocky
habitats in the lower intertidal zone on the Pacific coast of Costa Rica.
Several questions are addressed in this study: (1) What is the weight of sediments
accreted by individual sea cucumbers? (2) Is there a correlation between size or surface area of
the sea cucumber and total sediment load carried? (3) What is the composition of sediment types
carried by sea cucumbers? (4) Does the weight or composition of sediments vary with respect to
body region (head, median, posterior)? (5) Is the sediment load composition carried by the study
species a random subset of sediments available, or are the sea cucumbers selective?
STUDY SITE
Sea cucumbers were collected in the rocky intertidal zone at the San Miguel Biological
Station in Cabo Blanco Absolute Reserve in Costa Rica (N 09° 34.711, W 85° 08.235). Cabo
Blanco is on the Pacific coast at the southern tip of the Nicoya Peninsula, Puntarenas Province.
Tides are semidiurnal, with two high tides and two low tides per 24-hour period; the maximum
tidal range from low to high tide is 3 m or more.
The extensive rocky intertidal zone is made up of a relatively level wavecut platform
broken up by a network of narrow crevices, channels, ridges, and tidepools (Figure 1). The solid
rock substrates are predominately composed of turbidite, limestone, and sandstone. Within the
channels and tidepools are strewn smaller particles, including cobbles, gravel, pebbles, shells and
shell fragments, and sand.
Rainfall ranges from 2500 mm to 3200 mm, with little variation between years; the
distribution of rainfall during the year is highly seasonal, with approximately 95-100% percent of
44
the annual total falling during the May-November wet season (Lindquist 2003, Lindquist &
Carroll 2004). Discharge of cold water from streams and surface runoff of rainwater affects
temperature and salinity of water in tidepool habitats, especially during the rainy season.
The Quebrada San Miguel is the principal source of freshwater discharge into the
intertidal area. During dry periods, with little or no rainfall, the San Miguel stream is fed by
springs. A sandy berm develops at the mouth of the San Miguel, and discharge into the intertidal
zone is limited to the small volumes of clear freshwater that seep through the berm. When heavy
rainstorm events occur during the wet season, the stream quickly swells with runoff from the
surrounding hills, leading to breakthrough of the berm at the mouth of the stream, and bringing
large volumes of turbid, fast-moving, sediment-laden streamwater into the intertidal zone. In the
wake of such storms, the shore is strewn with logs, branches, decomposing leaf litter, gravel, and
sediments that have been washed from land and deposited in the intertidal area.
STUDY SPECIES
Holothuria inornata was first described by Semper (1868). The species is large, reaching
20 cm or more in length, and has a thick, leathery skin covered in papillae; its color is blackish
with a dark reddish tinge. Deichmann (1938) describes the main morphological and anatomical
characteristics of the species. Typical individuals, with and without the coating of sediments,
are shown in Figure 2.
Body wall ossicles in sea cucumbers are known to vary from species to species, and may
be used as an aid to identification. We carried out an examination of the body wall ossicles of
the sea cucumber in our samples following a standardized procedure (Hickman 1998). The
protocol for extraction and preparation of body wall ossicles is described in Appendix 1; a
description of the types of ossicles encountered in our samples is given in Appendix 2.
Certain sea cucumbers, including H. inornata, are prized as food by humans. Although
Costa Rica has enacted a total ban on sea cucumber fishing (Toral-Granda 2008), in the early
1990s there were reports of commercial fishing of this species in Costa Rica (Anonymous 2006).
METHODS
Sea cucumber collection and sediment analysis
Thirty full-grown sea cucumbers were collected from the study site from June-July 2012
during low tide. Each sea cucumber was photographed in situ on its home substrate and then on
a 5 mm grid to provide scale. Collected sea cucumbers were placed in individually numbered
plastic bags with a small amount of sea water for transport to the laboratory.
In the laboratory, length, width, and height of sea cucumbers were measured. From these
data, the estimated surface area of the back of each sea cucumber was calculated according to the
formula:
(
).
45
All sediments were scraped from the backs of the sea cucumbers with forceps in three
equal areas: head, median, and posterior of the sea cucumber (Figure 3). Sediments dropped
from the sea cucumber during transport or following transfer of the sea cucumber to its aquarium
in the laboratory were retrieved and included as part of the total sediment load for that
individual.
Collected sediment loads were dried to constant weight in a drying oven at 65° C.
Dried sediments from each individual were sorted according to five categories: sand,
shell, pebble, leaf, and unclassified. “Sand” included all particles small enough to pass through a
U.S.A. Standard Testing Sieve, Number 25 (opening of 710 micrometers). “Shell” included
whole shells as well as shell fragments. “Pebble” included small pebbles and rocks up to 4.8 cm
in diameter. “Leaf” included fragments of leaf litter. “Unclassified” materials comprised
miscellaneous particles that were too large to pass through the sieve and were too finely
comminuted to be readily recognizable as shell, pebble, or leaf material.
All sorted samples were then weighed to the nearest 0.1 g using Pesola spring scales. We
used the weights of the different sediment types to determine the total weight and percent
composition of the sediment load of each sea cucumber.
Analysis of background substrates
Substrate compositions in the field were analyzed by randomly dropping points in the
areas of the intertidal zone where sea cucumbers are found, and recording the type of sediment
hit. Of 782 points, 435 (56%) hit particulate substrate materials that could potentially be picked
up by sea cucumbers. Those were divided into categories matching the ones used in the analysis
of sediments borne by sea cucumbers (shell, pebble, sand, and leaf). Percent cover (and 95%
confidence intervals) were determined for each sediment type in the field.
The composition of substrates in the field was compared with the composition of
substrate materials carried by sea cucumbers in order to test whether or not sea cucumbers were
accreting a random subset of materials available.
RESULTS
Sea cucumber allometry
The sea cucumbers in our samples ranged in length from 94-193 mm (mean = 134 mm).
Surface area of the backs of the sea cucumbers ranged from 3,248-13,477 mm2 (mean = 7290
mm2). Length of the sea cucumbers was positively correlated to their width (r=0.571, 27 d.f.;
P<0.01) (Figure 4). Length was also positively correlated to the surface area of the back of the
animal (r=0.910, 27 d.f.; P<0.001) (Figure 5).
46
Analysis of sediments carried by sea cucumbers
The total weight of sediment removed from the sea cucumbers ranged from 1.3 g to 23.7
g (mean = 9.4 g) (Figure 6). The weight of the sediment load was independent of the surface
area of the back of the individual sea cucumber (r=0.145, 27 d.f.; P>0.05) (Figure 7).
The mean composition of sediments, taking into account the three principal sediment
types, was 45% shell, 30% pebble, and 25% sand (Figure 8). The sediment composition varied
greatly from individual to individual, and many sea cucumbers departed markedly from the mean
in the relative frequency of accreted materials. Individual compositions ranged, for example,
from 16% shell, 69% pebble, and 15% sand, to 68% shell, 18% pebble, and 14% sand, and 33%
shell, 1% pebble, and 66% sand.
The occurrence of different sediment types on the three different body regions was
evaluated using a contingency table (Table 1). We found no association between the presence or
absence of shells, pebbles, sand, or unclassified sediment and the body region of the sea
cucumbers (G=1.498, 6 d.f., P>0.05).
The weight of different sediment types was compared among the three body regions.
There was no difference among body regions in the weights of shell (n=30, P>0.05) (Figure 9),
pebble (n=30, P>0.05) (Figure 10), sand (n=30, P>0.05) (Figure 11), or unclassified materials
(n=30, P>0.05) (Figure 12). Sea cucumbers carry roughly the same materials over their entire
body.
A comparison was done of the total weights of shell, pebble, sand, and unclassified
materials for each of 30 individuals (Figure 13). The sea cucumbers carry less sand than shell by
weight (n=30, P<0.05), but all other substrate comparisons are the same (n=30, P>0.05).
Analysis of background sediment
The mean percent cover (and 95% confidence limits) were determined for the substrate
compositions in the field, based on the point sampling (n=435 samples) of the sea cucumbers’
habitat. The highest cover values were found for pebble, with 38% (33.02-43.26%), and sand,
with 38% (33.02-43.26%). Shell had significantly lower cover than either pebble or sand, with
24% (19.74-28.81%). Leaf litter was not found in the sample, for a cover of 0% (0.00-1.12).
In order to determine whether sea cucumbers make use of a random subset of sediments
available in their environment, we compared the % cover of substrates in the field with the mean
percent composition of sediments removed from the sea cucumbers. As seen in Figure 14, the
makeup of materials accreted by sea cucumbers departs markedly from that available in the field.
The mean percent by weight of shell among sea cucumber sediment loads was 45%. We
used a simulation approach to generate a probability density function, to determine the
probabilities associated with random sampling around an expected value of 45%. To create the
null distribution, we produced 20,000 simulation runs of 100 random draws each.
47
The modeled distribution establishes that the 99.99% confidence limits for the percent of
shell expected on the sea cucumbers, based upon the actual expected mean shell composition on
the sea cucumbers ranges from 30-61% shell. This is clearly outside the range of shell percent
cover that was found from point sampling in the field (Figure 15); hence the composition of
sediments on sea cucumbers does not reflect availability of materials in the environment, but
rather indicates selectivity on the part of the sea cucumbers.
Uncontrolled results: Post-storm samples
During low tide on the morning of 18 July 2012, heavy rain caused a washout of the berm
at the mouth of the Quebrada San Miguel, releasing large amounts of fresh water, sediment, and
leaf litter into the study area. During low tide on the morning of 19 July 2012, approximately 24
hours after the berm washout, we collected 40 sea cucumbers in a follow-up sample and recorded
the presence or absence of sediment types (shell, pebble, leaf, sand) on each.
Leaf fragments, which had been found on only one sea cucumber in the initial samples,
were present and abundant on all 40 of these individuals. Large quantities of leaf litter were
noted in tidepools, on the intertidal rocks, and floating on the surface of the water. In a
comparison of leaf materials carried by sea cucumbers before and after the berm break, we found
a strong association between the presence or absence of leaves as part of the sediment load and
the time of sampling (before or after the breaking of the berm) (G= 39.09, 1 d.f.; P<0.001 )
(Table 2).
On 2 August 2012, 15 days following the berm washout, a short visit was made to the
study site, at which time 11 individuals of H. inornata were encountered; all still bore a
substantial cover of leaf material, although leaves were no longer evident in the water column or
on the rocky substrates (D. Lieberman, personal communication).
DISCUSSION
There was great variability in how much, and in what composition, sediments were
carried by sea cucumbers. The range of individual variation among adult sea cucumbers
suggests that there may not be one combination of sediment that is preferred or is inherently
better than the others.
The lack of an association between body region and presence of different substrate types
confirms that sea cucumbers carry roughly the same composition of sediments across their entire
bodies.
Weight was considered the best measure for determining composition of sediments on the
sea cucumbers. Because different sediments have different densities, however, the estimates of
composition based on weight may not coincide with estimates based on presence and absence of
sediment types or estimates of percent cover. For example, we found that significantly less sand
was carried by weight than shell, and yet sand was the only sediment type that occurred on every
body region on every sea cucumber. The difference is likely to have arisen because of the
weight difference in a grain of sand and a fragment of shell.
48
The most interesting trends are seen when all of the data are evaluated in relation to one
another (Figure 12). The 95% confidence interval for the true observed composition of shell in
the sea cucumbers’ environment and the 99.99% confidence interval for the percentages of shell
predicted from random draws around our observed compositions do not overlap. This refutes the
null hypothesis that sea cucumbers are randomly pulling sediment from their environment.
Rather, it indicates that sea cucumbers have a preference for shells, since they carry them in a
higher proportion, in general, than they occur in the environment.
Additionally, there is strong evidence of individual preference. There were individual sea
cucumbers that were far from the mean composition. There were shell percentages for
individuals that were both above and below the 99.99% confidence intervals based on the mean.
Since all sea cucumbers were captured in the same region of the intertidal zone, they all would
have had access to the same sediments. This much variation cannot be explained by chance
alone.
The storm event which led to the washout of the berm and the release of the sediment and
dead leaf matter into the ocean allowed us to see how the sea cucumbers react when a foreign
material is in their environment. Previously, one sea cucumber had carried a single piece of
decomposing leaf material. Within two tidal cycles after the berm break, every sea cucumber
had incorporated leaf matter into the sediments carried.
The point samples to determine available sediment composition were done approximately
48 hours (four tidal cycles) after the berm washout, and although leaf material was visible and
apparent, the fraction was still quite low; the estimated 95% confidence intervals for leaf litter on
the ocean floor in the intertidal zone was 0.00-1.12%. Unfortunately, we were only able to
observe the environment at low tide and cannot speak to the state of the ocean floor at high tide.
It is possible that leaves were more available to the sea cucumbers during that time.
This study has shown that sea cucumbers are selective in their use of substrate materials
and do not pick up sediments in proportion to their availability. The basis for the selectivity is
not clear. Why do the sea cucumbers carry shell in a higher proportion than it occurs in the
environment?
We also would be interested to discover the mechanism by which the sea cucumbers
acquire the sediment and attach it to their bodies. We know from observation that the sediments
are held to the backs of the sea cucumbers by their tube feet. We do not know if the sea
cucumbers actively pick up these sediments, or if sea cucumbers only attach sediments that have
settled out of the water onto their backs. Laboratory and field trials have shown conclusively
that these sea cucumbers do not take up sediments upon which they are lying (Jackson, Nygaard
& Tejeda, personal observation).
Finally, and possibly of the most ecological importance, what caused the sea cucumbers
to take up leaves so readily? If sea cucumbers were taking up materials passively, in quantities
representative of their presence in the environment, then the sudden influx might explain their
rapid uptake. However, the fact that they retained leaves long after leaf fragments had
49
disappeared from the environment suggests that leaf acquisition was selective, and that leaves
might be a preferred type of material.
If sea cucumbers are as selective in their use of cover materials as is indicated in this
study, the question arises whether sea cucumbers are able to recognize and reject unnatural
materials such as pollutants that might enter their habitat. Determining whether or not the
sediment preference of sea cucumbers extends to selecting against unnatural materials could be
an important factor in protecting sea cucumber populations around the world.
ACKNOWLEDGEMENTS
We thank the participants and instructional staff of the 2012 CSU-LSAMP program, who
helped with the project in many ways. Editorial assistance and statistical consultation was
provided by Diana Lieberman of California State University Monterey Bay and Milton
Lieberman of the Ministry of the Environment (MINAET), Costa Rica. Support for this research
was provided through the Chancellor´s Office of the California State University and NSF grant
HRD-0802628 from the LSAMP program of the National Science Foundation. Programmatic
funding was made available by CSU-Monterey Bay’s SEP.org.
LITERATURE CITED
ANONYMOUS. 2006. National Report – Costa Rica. In Bruckner, A.W. (ed.), Proceedings of
the CITES workshop on the conservation of sea cucumbers in the families Holothuriidae and
Stichopodidae. NOAA Technical Memorandum NMFSOPR 34, Silver Spring, MD. 244 pp.
DIECHMANN, E. 1938. Holothurians from the western coasts of Lower California and Central
America, and from the Galápagos Islands. Eastern Pacific Expeditions of the New York
Zoological Society. XVI. Zoologica (NY) 23: 361-387.
GRAHAM, D., & MIDGLEY, N. 2000. Tri-plot (v. 1.4.2) [computer software]. Loughborough,
UK: Loughborough University. Retrieved 5 December 2012. Available from
http://www.lboro.ac.uk/research/phys-geog/tri-plot/index.html
HICKMAN, C.P., JR. 1998. A field guide to sea starts and other echinoderms of Galápagos.
Galápagos Marine Life Series. Sugar Spring Press, Lexington, VA. 83 pp.
HYMAN, L.H. 1955. The Invertebrates: Echinodermata. Vol. 4. McGraw-Hill, New York,
NY. 763 pp.
LINDQUIST, E.S. 2003. Patterns of coastal forest composition, structure and recruitment,
Costa Rica: Functions of an environmental gradient, seed rain distribution, and crab predation
pressure. Ph.D. Dissertation, University of Georgia, Athens, GA. 188 pp.
LINDQUIST, E.S. & CARROLL, C.R. 2004. Differential seed and seedling predation by crabs:
impacts on tropical coastal forest composition. Oecologia 141: 661-671.
50
MOSHER, C. 1956. Observations on evisceration and visceral regeneration in the sea-
cucumber, Actinopyga agassizi Selenka. Zoologica (NY) 41: 17-26.
SEMPER, C. 1868. Reisen im Archipel de Philippinene, Pt. 2, vol. 1, Holothurien, pp. 1-288,
pls. 1-40.
TIMM, R.M., LIEBERMAN, D., LIEBERMAN, M. & McCLEARN, D. 2009. Mammals of
Cabo Blanco: history, diversity, and conservation after 45 years of regrowth of a Costa Rican
dry forest. Forest Ecology & Management 258: 997-1013.
TORAL-GRANDA, V. 2008. Population status, fisheries and trade of sea cucumbers in Latin
America and the Caribbean. Pp. 213-229 in Toral-Granda, V., Lovatelli, A. and Vasconcellos,
M. (eds.), Sea cucumbers. A global review of fisheries and trade. FAO Fisheries and
Aquaculture Technical Paper. No. 516. Rome, FAO.
VANDENSPIEGEL, D. & JANGOUX, M. 1987. Cuvierian tubules of the holothuroid
Holothuria forskali (Echinodermata): a morphofunctional study. Marine Biology 96: 263-275.
VANDENSPIEGEL, D., JANGOUX, M. & FLAMMANG, P. 2000. Maintaining the line of
defense: regeneration of Cuvierian tubules in the sea cucumber Holothuria forskali
(Echinodermata: Holothuroidea). Biological Bulletin 198: 34-49.
Table 1. Distribution of four principal sediment types among the three body regions of 30 sea
cucumbers. There is no association between the presence of sediment type and body region
(G=1.498, 6 d.f.; P>0.05).
Head Median Posterior Total
Shell 28 24 27 79
Pebble 14 18 21 53
Sand 30 30 30 90
Unclassified 25 25 29 79
Total 97 97 107 301
51
Table 2. Presence or absence of leaves on sea cucumbers sampled before and after the storm that
caused the washout of the berm. There is a strong association between leaf presence and the time
of sampling (G=39.09, 1 d.f.; P<0.001); following the storm, all sea cucumbers sampled carried
leaves.
Before Storm After Storm Total
Leaf Present 1 40 41
Leaf Absent 29 0 29
Total 30 40 70
Figure 1. Typical lower intertidal rocky habitat of Holothuria inornata. At low tide, sea
cucumbers are found in shallow pools, moist rock crevices or under overhanging ledges of rock.
52
(a)
(b)
Figure 2. Individuals of the sea cucumber H. inornata (a) with typical coating of sediments
including sand grains, shell fragments, small pebbles, and small leaf fragments and (b) with all
sediment particles removed and the dark red skin and surface papillae visible on the back of the
animal.
Figure 3. Removal of sediments from the back of an individual sea cucumber in the laboratory
in preparation for drying and weighing.
53
Figure 4. Allometric relationship between body length and body width in a sample of 29 sea
cucumbers. The length and width are positively correlated. (r=0.571, 27 d.f.; P<0.01)
Figure 5. Allometric relationship between body length and surface area of the back in a sample
of 29 sea cucumbers. The length of a sea cucumber is positively correlated with the surface area
of its back (r=0.910, 27 d.f.; P<0.001).
0
10
20
30
40
50
60
70
0 50 100 150 200 250
Wid
th (m
m)
Length (mm)
0
2000
4000
6000
8000
10000
12000
14000
16000
0 50 100 150 200 250
Surf
ace
are
a (m
m2
)
Length (mm)
54
Figure 6. Frequency distribution of total weight of sediment loads for a sample of 30 individual
sea cucumbers.
Figure 7. Relationship between the surface area of the back of a sea cucumber and the total
weight of the sediment load carried. Sediment load is independent of surface area (r=0.145, 27
d.f.; P>0.05).
0
1
2
3
4
5
6
7
8
2 4 6 8 10 12 14 16 18 20 22 24 More
Nu
mb
er
of
ind
ivid
ual
s
Total sediment weight (g)
0
5
10
15
20
25
0 2000 4000 6000 8000 10000 12000 14000 16000
Tota
l sed
imen
t lo
ad (
g)
Surface area (mm2)
55
Figure 8. Composition of sediment loads (three principal sediment types only) carried by each
sea cucumber (filled circles). Percent composition based on weight. Bottom scale: % Shell; left-
hand scale: % Pebbles; right-hand scale: % Sand. The mean composition (open circle) was 45%
shell, 30% pebble, and 25% sand. Graph made using Tri-plot (Graham and Midgley 2000).
100 90 80 70 60 50 40 30 20 10 0
56
Figure 9. Total weights (g) of shell taken from three body regions of 30 sea cucumbers; means
and 95% confidence limits are shown. Body regions: head (H Sh), median (M Sh), and posterior
(P Sh). Based on a comparison of confidence limits, there was no difference among the body
regions in the weight of shell carried (P>0.05).
Figure 10. Total weights (g) of pebble taken from three body regions of 30 sea cucumbers;
means and 95% confidence limits are shown. Body regions: head (H Pb), median (M Pb), and
posterior (P Pb). Based on a comparison of confidence limits, there was no difference among the
body regions in the weight of pebble carried (P>0.05).
0.000
0.050
0.100
0.150
0.200
0.250
0.300
0.350
0.400
0.450
0.500
H Sh M Sh P Sh
Tota
l we
igh
t o
f sh
ell
(g)
Body region
0.000
0.020
0.040
0.060
0.080
0.100
0.120
0.140
0.160
0.180
0.200
H Pb M Pb P Pb
Tota
l wei
ght
of
peb
ble
(g)
Body region
57
Figure 11. Total weights (g) of sand taken from three body regions of 30 sea cucumbers; means
and 95% confidence limits are shown. Body regions: head (H Sa), median (M Sa), and posterior
(P Sa). Based on a comparison of confidence limits, there was no difference among the body
regions in the weight of sand carried (P>0.05).
Figure 12. Total weights (g) of unclassified materials taken from three body regions of 30 sea
cucumbers; means and 95% confidence limits are shown. Body regions: head (H Un), median (M
Un), and posterior (P Un). Based on a comparison of confidence limits, there was no difference
among the body regions in weight of unclassified materials carried (P>0.05).
0.000
0.050
0.100
0.150
0.200
0.250
0.300
0.350
0.400
0.450
H Sa M Sa P Sa
Tota
l we
igh
t o
f sa
nd
(g)
Body region
0.000
0.050
0.100
0.150
0.200
0.250
0.300
0.350
H Un M Un P UnTota
l wei
ght,
un
clas
sifi
ed
mat
eri
als
(g)
Body region
58
Figure 13. Total weights (g) of shell, pebble, sand, and unclassified materials taken from 30 sea
cucumbers; means and 95% confidence limits are shown. Leaf material is not included; leaf was
found on only one individual, and its weight was too small to measure. Sea cucumbers carry
more shell than sand (P<0.05), but all other comparisons are equal (P>0.05).
Figure 14. Comparison of percent cover of available substrate from field samples (closed circles
with 95% confidence limits) and percent composition of sediments found on sea cucumbers
(open circles). Sediments used by sea cucumbers are not representative of those present in the
field, indicating that sea cucumbers are selective in their acquisition of sediments.
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
4.0
4.5
Shell Pebbles Sand Unclassified
Tota
l wei
ght
(g)
Sediment type
0
10
20
30
40
50
60
Per
cen
t co
mp
osi
tio
n
Shell Pebble Sand
Sediment type
59
Figure 15. Use of a simulation model to compare the percent of shell on sea cucumbers (pooled
value 45%) and the percent cover of shell in the field. A null probability density function
(simulation model) was created by repeated sampling (n=20,000 runs of 100 random draws each)
around an expected value of 45%, simulating a random draw from the pooled sea cucumber data.
The 0.001 probability levels occur at ≤ 30% shell (lower limit) and ≥ 61% shell (upper limit).
Point sampling of shell substrates in the field (24%) is shown with 95% confidence limits (19% -
28%). These distributions do not overlap, showing that sea cucumbers carry shell in a
substantially higher proportion than it occurs in the environment. Individual sea cucumbers also
bore quantities of shell that were outside the 0.001 probability limits, confirming the substantial
variability in choice of sediments from one animal to the next.
0
0.01
0.02
0.03
0.04
0.05
0.06
0.07
0.08
0.091 5 9
13
17
21
25
29
33
37
41
45
49
53
57
61
65
69
73
77
81
85
89
93
97
101
Freq
uen
cy
Percent shell
Sea cucumbers, simulation model, mean percent
Low
er
limit
, sim
ula
tio
n m
od
el, P
=0.0
01
Up
per
lim
it, s
imu
lati
on
mo
del
, P=0
.00
1
Low
er
limit
, sim
ula
tio
n m
od
el, P
=0.0
1
Up
per
lim
it, s
imu
lati
on
mo
de
l, P
=0
.01
Field samples,
mean percent ±
95% confidence
limits
60
Appendix 1. Extraction and preparation of sea cucumber body wall ossicles.
(Method follows Hickman 1998)
Materials
Scalpel or razor blade
Medicine dropper or pipette; small test tubes
Compound microscope; microscope slides and cover slips
Commercial household bleach
Extraction and Preparation Protocol
1. A thin piece of tissue approximately 1 millimeter thick and 1 square centimeter in area is
sliced from the body wall of the sea cucumber with a sharp scalpel or razor blade.
2. The slice of body wall tissue is dropped into a small test tube, and 1-3 ml of commercial
bleach is added.
3. The test tube is allowed to stand for 30-60 minutes until the tissue is dissolved; the ossicles
will have fallen to the bottom of the test tube as fine white sediment.
4. The supernatant is carefully removed with a medicine dropper or pipette, taking care not to
disturb the precipitated sediment. Clean water is added.
5. After the sediment has settled for a few minutes, some of the white sediment is transferred to
a blank microscope slide with a pipette or medicine dropper, and a cover slip is added. The
sample is examined with a compound microscope at 100x power.
6. If tissue samples are to be stored, they may be placed in 70% alcohol for storage.
7. The extraction of body wall ossicles by this method causes no lasting harm to the sea
cucumbers, which are returned to the environment following the procedure.
Appendix 2. Illustration of body wall ossicles extracted from Holothuria inornata.
Sea cucumber ossicles are classified according to their general shape, using the following
categories (Hickman 1998): Table: perforated disc with a spire made up of (usually) four rods
joined by crossbars. Button: flattened, elongate perforated bodies; may be smooth or knobbed.
Rosette: tiny ossicles made up of branching rods in a single plane. Rod: elongate bars,
sometimes perforated on the ends; these serve as supporting structures in the tube feet and
tentacles of the sea cucumber. Perforated plate: sievelike in form, often quite large in relation
to other kinds of ossicles; common in many species of sea cucumbers.
In the current study, ossicles were extracted from the body wall of a single individual of H.
inornata following the protocol described above. Examination of prepared samples revealed the
presence of tables and rods (Figure 16).
61
Figure 16. Photomicrograph of body wall ossicles sampled from Holothuria inornata. The
ossicle types seen in the image are tables and rods.
62
Comparison of protected and exploited tooth shell (Nerita scabricosta)
populations on the Pacific coast of Costa Rica
JENNIFER RETANA1, EMILY ESCOBAR
2 & DWAYNE FRANCO
3
1Department of Biology, California State University Los Angeles, Los Angeles, CA 90032
2Department of Biology, California State University San Bernardino, San Bernardino, CA
92407 3Division of Science & Environmental Policy, California State University Monterey Bay,
Seaside, CA 93955
ABSTRACT. Tooth snails, Nerita scabricosta (Gastropoda: Neritidae), are gathered for
food along the Pacific coast of Costa Rica. Snails occur on both raised vertical faces and
low-lying, horizontal surfaces of rocky intertidal benches. We assessed snail density, size
distribution, and spatial dispersion pattern of these snails during daytime low tides, when
snails were inactive, at three sites with progressively decreasing levels of protection from
human access: (1) San Miguel Biological Station in the Cabo Blanco Absolute Reserve,
closed to the public since 1963; (2) Playa Los Suecos, an area of limited public access just
north of San Miguel Biological Station, and (3) Los Banquillos, an area open to the
community and the public at large located north of Playa Los Suecos and approximately 3
km north of San Miguel Biological Station.
In Cabo Blanco, Nerita was also sampled during a cool, evening low tide, when
snails were actively grazing.
Mean density ranged from 3.4–7.8 individuals per 0.25 m2 quadrat (13.6-31.2/m
2
during periods of inactivity, and reached a maximum of 19.5 individuals per quadrat
(78.0/m2) when snails were actively grazing. Snail density on vertical faces was
equivalent at all three sites. On horizontal habitats, density was higher at Los Suecos than
at the other two sites.
Snails in all three sample areas consistently showed a clumped spatial dispersion
pattern. In addition, snails were not randomly mixed with respect to size, but tended to
group themselves with other individuals of comparable size.
Nerita snails ranged in diameter from 0.2-3.7 cm. Large snails tended to occur on
exposed vertical rock faces, and were less often found on horizontal habitats.
63
Rates and consequences of water loss were studied experimentally in a sample of
snails exposed to air drying; weight loss was used as a surrogate for water loss. Rates of
water loss did not vary with size, but larger snails remained active longer in the absence
of re-wetting than did smaller snails. Water loss from live snails occurred much more
slowly than water loss from comparable samples of dead snail tissue; live snails reduced
water loss behaviorally by closing the operculum and remaining inactive during the day.
The difference in Nerita size distribution between lower horizontal surfaces and exposed
vertical faces may be explained in part by the relative resistance to water loss among large
snails.
The largest snails, the highest density of snails, and the greatest biomass of snails
per unit area were present in Cabo Blanco, where no collecting was permitted. Large
snails were fewest in the area where the public had unlimited access, and an intermediate
density of large individuals was present where limited access was permitted. This study
suggests that exploitation of the snails outside the reserve has affected unprotected Nerita
populations, and that protection of this species within the reserve has been effective.
INTRODUCTION
The distribution and abundance of marine invertebrates living within the rocky
intertidal may be affected by natural pressures (salinity, temperature, solar radiation,
water movement, food availability, and predation) as well as anthropogenic pressures
alteration of coastal morphology, pollution, and extraction of marine resources, especially
for food (Cortes & Wehrtmann 2009). Human settlement in coastal areas worldwide has
led to the fragmentation, disturbance and transformation of marine inshore ecosystems.
Parks and reserves in coastal areas serve to protect habitat, act as reservoirs for plant and
animal populations, and preserve the natural functions of these interconnected
communities. In particular, protected areas provide an important refuge for edible marine
intertidal species (Ortega 1987, Pombo & Escofet 1996, Sagarin et al. 2007).
The marine biodiversity of Costa Rica and its conservation have been reviewed
recently by Wehrtmann & Cortes (2009). Costa Rica is considered to be a leader in
conservation and habitat protection; roughly 25% of its land surface is under protection in
parks and reserves. A total of 30,308 km2 is registered in marine protected areas (Cortes
& Wehrtmann 2009); this represents around 16.5% of the Internal Waters and Territorial
Seas (SINAC-MINAE 2006).
Reserva Natural Absoluta Cabo Blanco on the Pacific coast protects
approximately 1,270 ha of terrestrial area and 1,629 ha of marine environment (Cortes &
Wehrtmann 2009). Terrestrial habitats of the reserve have been closed to public access
since the park was established in 1963, and the shore and marine area starting in 1985.
Since then, access by the public to intertidal areas has been strictly prohibited. Collection
of shellfish and fishing in the area is not allowed (Timm et al. 2009).
64
Tooth shells, Nerita scabricosta (Gastropoda: Neritidae) are common inhabitants
of the rocky intertidal of the tropical eastern Pacific, extending from the Gulf of
California to the outer Pacific coast of southern Baja California to Ecuador. (Hurtado et
al. 2007). The species, which grazes algae, is found throughout the intertidal, ranging
from lower and middle levels to the highest sunbaked rocks in the splash zone where the
snails are wetted only at high tide (Keen 1971, Mena Aguilar 1995). They occupy both
level, low-lying horizontal rocky platforms and vertical faces of uplifted rock outcrops.
Mena Aguilar (1995), in his survey of intertidal invertebrates in Cabo Blanco reports that
the species is “very abundant” in both the middle and upper intertidal zones.
Identification of the study species, Nerita scabricosta Lamarck 1822 is based on
Keen (1971); taxonomic status was confirmed following Rosenberg (2012). Shells of this
species (Figure 1) are globular in shape and low-spired, featuring an outer lip which is
toothed, and an oddly-shaped calcareous operculum that effectively seals in moisture
when the animal is exposed to the air during low tides (Keen 1971).
Tooth snails (known as “burgados”) are prized as food and gathered at low tide by
local people along the Pacific coast of Costa Rica, who marinate them in lime juice to
make ceviche, boil them and serve them with garlic butter, or prepare them in a rice dish
(“arroz con burgados”). Large snails are preferred; snails less than 1cm in diameter are
not taken, as the yield of edible flesh is so small (Luz Marina Gomez, personal
communication).
If exploitation of tooth snails is done at a sustainable level, such that the harvested
snails are replaced by recruitment of smaller size classes, the population density and size
class distribution should be maintained in a steady state. If collection is not done
sustainably, then the density and size distribution should reflect the impact of human
activity, and areas with differing levels of exploitation should show differences in the
snail demography.
Studies of edible intertidal snails elsewhere have documented such effects.
MacGinitie & MacGinitie (1949) noted that the intertidal turban Tegula in Monterey, CA
“became smaller and scarcer year after year” because they were sought after for food.
Ricketts et al. (1985) remarked on the decline of tasty intertidal snails that are harvested in
California, notably the giant owl limpet Lottia gigantea and the black turban Tegula
funebralis. Collecting of these snails in California is currently prohibited within marine
reserves, and is regulated elsewhere on the coast with a bag limit of 35.
We assessed snail density, size distribution, biomass and spatial dispersion
patterns of tooth snails inside and outside the Cabo Blanco Absolute Reserve, at three
sites with progressively decreasing levels of protection from human access. Data were
also collected on rates of water loss and tolerance to desiccation with respect to snail size.
65
METHODS
Sampling of tooth snails, Nerita scabricosta, occurred during daytime low tides,
while snails were inactive, over a ten-day period during June-July 2012. From the most
strictly protected to the least protected (Figure 2), the sites are: (1) San Miguel Biological
Station (9º 34′ 43″ N, 85º 08′ 12″ W), in the western sector of the Cabo Blanco Absolute
Reserve, with intertidal and marine habitats closed to the public since 1985, (2) Playa Los
Suecos (9º 35′ 42″ N, 85º 08′ 36″ W), at the northern end of the Reserva Cueva los
Murcielagos, 1.5 km north of the Cabo Blanco site, and (3) Los Banquillos (9º 36′ 35″ N,
85º 08′ 46″ W), on the open beach of Malpaís, 1.5 km north of Playa Los Suecos and 3
km north of the Cabo Blanco site.
Within each of the three sites, sampling was done separately on two kinds of rocky
intertidal habitats: low-lying, horizontal surfaces and vertical rock faces. At each site,
samples of Nerita were collected from a 0.25 m2 quadrat at random points along a transect
parallel to the shore approximately 20 to 30 meters seaward from the zone of contact
between the sandy beach and the edge of the rocky intertidal zone. Within each quadrat,
all visible Nerita individuals were collected, bagged, and returned to the laboratory where
they were counted, measured in diameter at the widest point with a dial caliper, and later
released (Figure 3).
A single followup set of samples was taken on 28 September 2012 during a cool,
early evening low tide, when snails were actively feeding. These samples were taken in
Cabo Blanco on horizontal rock habitats in the intertidal zone.
Figure 4 shows contrasting quadrat samples when Nerita was inactive (daytime
low tide) and active (evening low tide).
To determine rates and consequences of water loss in relation to size, Nerita snails
were collected in San Miguel and divided into five weight classes: 0-4 g; 5-9 g; 10-14 g;
15-19 g; and ≥ 20 g. Prior to the start of the water loss trials, the snails were kept in a
large plastic tub with ample sea water and large rocks; during this period of acclimation,
the snails attached themselves to the rocks and sides of the tub, and were fully hydrated,
having freely taken up normal amounts of sea water into the mantle cavity (Figure 5).
As each Nerita was removed from the tub, a small plastic cup was placed beneath
it in order to capture any water released by the snail as a stress response. The weight (g)
of water released by the snail was added to the weight of the snail in order to obtain the
total initial wet weight of the snail.
A piece of thin nylon string approximately 30 cm in length was attached to the
shell of each snail with super glue (Figure 6), after which the individual was re-weighed
to obtain the total weight of the snail, glue, and string. Each snail was hung to dry in the
open air under the roof overhang of a storage shed located under partial forest shade
approximately 20 m from the
66
shore. The weight of each of the 50 Nerita snails was measured at time intervals over a period
of 400 hours, or approximately 17 days. At the time of weighing, snails were scored on a scale
of 1-5 with regard to activity level.
A similar process was conducted to determine rates of water loss for tissue
extracted from dead Nerita snails. We collected the same number of snails in each weight
class as were used in the previous trials, and used a bench-top vise to crush the snail shells
and extract the snail tissue from the shells. Upon removal, the tissue samples were
weighed, and then hung from a wire using needle and thread. Samples were weighed at
intervals over a period of about 70 hours, or approximately 3 days.
Environmental conditions on site (air temperature, relative humidity and wind
speed) were recorded during the drying trials. Air temperature ranged from 26.2 to
30.0ºC (mean = 28.25ºC); relative humidity ranged from 95 to 100% (mean = 99.5 %);
and winds ranged from calm conditions to moderate breezes; wind speeds remained less
than 7 m/sec during the time of the study.
Local residents encountered at the sampling sites were interviewed informally to
obtain information on harvesting practices, preferred collecting sites, and use of the snails.
RESULTS
Density
The density (number of individuals per 0.25 m2 quadrat) was analyzed for each of
the three sampling sites and each of the two rocky habitats within each site. The density
frequency data, which are strongly right-skewed, were first transformed with a square-
root transformation: d′ = √ (d + 0.5), in which d is density and d′ is the transformed
density value. Transformed data were then compared using Student’s t.
Differences in density were compared within sites between the vertical and
horizontal habitats. In each area examined, the density of snails on vertical surfaces of the
rocky intertidal was either greater than or equal to that on the horizontal locations. At
Cabo Blanco, density was higher in vertical habitats (mean=7.8 per quadrat) than in
horizontal habitats (mean=3.4) (t=2.129, 279 d.f.; P<0.05). At Los Suecos, densities did
not differ between vertical (mean=3.6 per quadrat) and horizontal (mean=6.6) habitats
(t=1.590, 271 d.f., P>0.1). At Los Banquillos, density was higher in vertical habitats
(mean=6.5 per quadrat) than in horizontal habitats (mean=3.4) (t=2.596, 281 d.f.; P<0.02).
Density comparisons were also made among the three sites. In horizontal habitats,
density of Nerita was higher at Los Suecos than at either Cabo Blanco (t=2.898, 456 d.f;
P<0.01) or Los Banquillos (t=3.666, 437 d.f.; P<0.001). Density on horizontal surfaces
did not differ between Cabo Blanco and Los Banquillos (t=1.06, 451 d.f.; 0.2<P<0.4).
67
On vertical habitats, snail density was equivalent at all three sites: density at Cabo
Blanco was equal to that of both Los Suecos (t=1.610, 94 d.f.; 0.1<P<0.2) and Los
Banquillos (t=0.439, 109 d.f.; 0.5<P<0.9). Likewise, there was no difference in density
between Los Suecos and Los Banquillos (t=1.380, 115.d.f.; 0.1<P<0.2).
A comparison of density values (number/m2) is shown in Figure 7.
Spatial pattern
Spatial dispersion pattern was analyzed for Nerita snails at each of the sites by
comparing the frequency distribution of snail density observed in replicate 0.25 m2
quadrats to that of the null Poisson model. The mean density and variance of density
were calculated, and the ratio of the variance / mean of density was compared with the
expected ratio (variance / mean = 1) for the Poisson distribution. The observed and
expected ratios were compared using a special t-test (Greig-Smith 1984), formulated as
follows:
t = (s2/mean) - 1
√ [2 / (n - 1)]
where n is the number of replicate quadrats in the sample and n-1 is the number of
degrees of freedom. The null Poisson model (variance=mean) implies a random
dispersion pattern, while rejection of the null hypothesis would imply either a clumped
(variance>mean) or hyperdispersed (variance<mean) pattern.
During daytime low tides, while snails were inactive, the dispersion of Nerita was
consistently non-random; a clumped spatial pattern was seen on both vertical and
horizontal surfaces at all three sites (see Figure 7). The ratio of the variance / mean in
Cabo Blanco was 20.524 on horizontal substrates (t=211.653, 235 d.f.; P<0.001) and
36.367 on vertical faces (t=165.887, 44 d.f.; P<0.001); at Los Suecos, the ratio was
34.021 on horizontal surfaces (t=347.137, 221 d.f.; P<0.001) and 13.726 on vertical faces
(t=63.623, 50 d.f.; P<0.001); and at Los Banquillos, the ratio was 37.053 on horizontal
surfaces (t=374.579, 216 d.f.; P<0.001) and 39.293 on vertical faces (t=218.310, 65 d.f.;
P<0.001).
Spatial pattern of Nerita was analyzed as well during an evening low tide, when
the snails had emerged from the shelter of crevices and overhanging ledges and were
actively grazing on the rocks; these samples were taken at Cabo Blanco on horizontal
substrates. Mean density within the quadrat samples was much higher, with 19.5
individuals per 0.25 m2 quadrat (or 78.0/m
2) (Figure 8). The snail dispersion pattern was
again clumped, although less strongly than during periods of inactivity; the variance /
mean ratio was 16.633 (t=77.380, 49 d.f.; P<0.001).
In all samples tested, Nerita individuals tend to occur close to one another more
often than would be expected by chance.
68
Size distribution
Size distributions of Nerita shells for each of the three sampling sites and each of
the two habitats within each site are shown in Figure 9. Snail diameter ranged from 0.2-
3.7 cm. The mean diameter of snails within the vertical habitat in Cabo Blanco
(mean=2.58 cm) was greater than that of either Los Suecos (mean=1.44 cm; t=10.548,
539 d.f.; P<0.001) or Los Banquillos (mean=1.38 cm; t=14.126, 771 d.f.; P<0.001).
There was no difference in snail size between Los Suecos and Los Banquillos on vertical
habitats (t=0.920, 612 d.f.; P>0.05).
The mean diameter of snails within the horizontal habitats in Los Banquillos
(mean=1.39 cm) was greater than that of either Cabo Blanco (mean=1.06 cm; t=10.491,
1519 d.f.; P<0.001) or Los Suecos (mean= 1.11 cm; t=-9.601, 2181 d.f.; P<0.001). Snail
diameter on horizontal surfaces did not differ between Cabo Blanco and Los Suecos
(t=2.986, 2298 d.f.; P>0.05).
Comparisons of Nerita size between vertical and horizontal habitats within each
site were also done. Vertical habitats had larger snails than horizontal habitats at Cabo
Blanco (t=18.120, 468 d.f.; P<0.001) and at Los Suecos (t=4.746, 1670 d.f.; P>0.001).
There was no size difference between vertical and horizontal habitats at Los Banquillos
(t=0.530, 1123 d.f.; P>0.05).
The maximum diameters of snails sampled at the three sites were as follows:
Cabo Blanco, 3.7 cm; Los Suecos, 3.0 cm; and Los Banquillos, 3.0 cm.
Grouping of individuals based on size
In order to test whether Nerita snails are randomly mixed with respect to size, or
alternatively whether they tend to sort themselves in the field according to size, diameter
distributions were analyzed within individual quadrats. The variance in size within each
quadrat was compared with the variance of size for all quadrats pooled. If the diameter
distribution within a single quadrat were a random subsample of the overall diameter
distribution, the variances would be comparable. Alternatively, if individual snails tended
to occur in groups with others of a similar size, the variance of diameter within each
quadrat would be lower than the variance of diameter of the quadrats pooled.
An F-test (one-tailed) was used to test the null hypothesis that the variance of an
individual quadrat was equivalent to the variance of the total pooled sample; the overall
variance was divided by the individual quadrat variance.
Included in the analysis were quadrat samples from horizontal substrates at Cabo
Blanco with 17 or more individuals. For samples taken during daytime low tides while
snails were inactive, 17 quadrat samples were analyzed (Figure 10). These were
compared with the diameter distribution of snails from all quadrats pooled (Figure 11).
69
For 15 (88%) of the quadrats tested, the individual quadrat variance was lower
than the overall total variance, indicating that Nerita snails, while at rest, tend to sort
themselves according to shell diameter, forming groups based on size.
For samples taken in the evening during periods of active feeding, 23 quadrat
samples were analyzed (Figure 12). These are compared with the size distribution of
snails from all quadrats pooled (Figure 13). For 19 (83%) of the quadrats tested, the
variance of the quadrat was lower than the overall variance, indicating that during periods
of activity, as well, Nerita snails tend to occur in groups with snails of similar size.
Biomass
Snail weight as a function of size was determined for a sample of tooth snails, and
the resulting regression equation was used to make an estimate of the biomass of snails
per unit area in each site. The relationship between snail diameter measured at the widest
part of the shell and the dry weight of snail tissue is shown in Figure 14.
As seen in Table 1, the greatest biomass was found in Cabo Blanco. The biomass
for the Cabo Blanco vertical habitat (80.98 g/m2) was greater than that of the horizontal
site (26.75 g/m2). The horizontal site for Los Suecos (52.67 g/m
2) was greater in biomass
than the vertical site (31.89 g/m2). In Los Banquillos, biomass on vertical habitats (54.41
g/m2) was greater than that on horizontal rock surfaces (27.60 g/m
2).
Snail weight and the release of water from the mantle cavity
When disturbed, handled or removed from the substrate, Nerita snails release the
water which is held in the mantle cavity. The ejected water was collected and weighed
for a sample of snails. There is a positive correlation (r=0.909, 48 d.f.; P<0.001) between
live snail weight (shell plus soft tissue) and the weight of water ejected by the snail
(Figure 15); larger snails release larger quantities of water. The relationship is described
by the regression equation y=0.0831x + 0.0624).
Water loss trials
The pattern of water loss over time is shown over a period of 400 hours
(approximately 16.7 days) for 10 individuals in each of five size classes of live Nerita
snails exposed to drying in the air (Figure 16). Weight loss was used as a surrogate for
water loss. The rates of water loss in live snails did not vary with size, but appear to be
similar for all size classes.
No mortality occurred in any size class during the 400-hour water loss trials,
however a reduction in activity level was noted among some of the snails. Inactivity was
seen most often in smaller snails. After 72 hours without re-wetting, inactivity was noted
in all 10 individuals of the smallest (≤ 4 g) size class, 7 of the 5-9 g class, 4 of the 10-14 g
class, 2 of the 15-19 g class, and none of the snails in the largest (≥20 g) size class.
70
Water loss over time for dead Nerita tissue exposed to air drying is shown in
Figure 17. Again, the rate of water loss in dead tissue appears independent of size class.
Based on the slope of the regression equation, a calculation of “half-life” of weight
loss was made, projecting the length of time over which 50% of the initial weight is
predicted to be lost. Values of half life are shown for live Nerita snails and dead snail
tissue in Table 2. The half-life of water loss for live snails (20.2-25.2 days) is an order of
magnitude longer than that for dead tissue (2.3-2.6 days).
DISCUSSION
Nerita consistently showed a clumped spatial dispersion pattern; this pattern was
noted at all sites on both horizontal and vertical surfaces. During daytime low tides, when
the snails were inactive, individuals were typically clustered tightly together in moist
crevices in the rock, in physical contact with one another. Garrity (1984), working in
similar habitat in Panama, found that aggregated snails maintained lower tissue
temperatures than non-aggregated snails; this may explain the tendency for Nerita to
cluster together on these shores.
A clumped dispersion pattern was also found among snails sampled during the
evening low tide, when they had emerged from the shelter of crevices and shade and were
actively feeding. In this case, the snails were not physically in contact with each other,
but were moving about the rocks in groups. This non-random pattern may arise because
suitable habitat, with adequate shelter and food, is not found homogeneously throughout
the habitat, but is itself patchy in its distribution.
Nerita individuals in the field are not randomly mixed with respect to diameter,
but tend to occur with others of a similar size. This segregation by size was found both
during periods of inactivity, when snails were packed into crevices and under shady
ledges, and during grazing periods, when snails were actively moving over the rocks. It is
unknown whether the size classes represent cohorts of the same age that settled together
and remain together as stable groups, or whether the snails are constantly mixing and re-
sorting themselves by size. The tendency for intertidal marine snails to occur in
aggregations based on size has been reported previously in the top shell Tegula funebralis
on temperate shores (Paine 1969, Morris et al. 1980, Ricketts et al. 1985), who remarked
that when size classes are mixed experimentally and released together in the field, the
snails re-establish their size groupings within one complete tidal cycle. An explanation
for this size-sorting behavior is lacking, and awaits further research.
While sampling outside the reserve on 27 June 2012 we noticed three families
collecting various marine animals, each with at least three members to help with the
harvesting. Interviews with people at the small fishing harbor just north of Los Suecos
indicated that local people prefer to collect snails from vertical uplifted rocks in the upper
intertidal zone, and that they prefer to do so at Los Suecos, our intermediate study site.
71
One resident mentioned a preference for collecting Nerita snails on the vertical
habitat of Los Suecos over that of any other site; he noted that he did so at least twice a
week during the day when weather conditions were ideal (Pablo Sanchez, personal
communication).
The rate of water loss by Nerita snails exposed to air drying was independent of
snail size; larger individuals lost water at the same rate as smaller individuals. However,
the effects of drying were higher in small snails during the water loss trials, as larger
snails remained active longer in the absence of re-wetting. In addition, larger snails
tended to release larger quantities of water when handled or disturbed, presumably
reflecting the larger capacity of the mantle cavity in larger snails. The difference in Nerita
size distribution between low horizontal surfaces and exposed vertical faces, with larger
snails tending to be found on vertical habitats, may be explained in part by the ability of
larger snails to retain comparatively larger amounts of water in the mantle cavity, which
may help resist dessication.
Water loss was much more rapid from dead snail tissue than from live snails. Live
snails were able to reduce desiccation by closing the operculum. When suspended in air,
they behaved in keeping with environmental conditions, venturing out of their shells at
night when temperatures were cool, and withdrawing into their shells and closing the
operculum during the day when temperatures were warm.
The distribution of tooth shells with respect to tidal height appears to reflect a
compromise between risks of predation by fish at lower levels in the intertidal zone and
exposure to heat and desiccation at higher levels. Large snails, which are better able to
tolerate the dry conditions on uplifted, vertical faces and are thus able to escape predation
by fish, are especially vulnerable to exploitation by humans where harvesting is permitted.
Cabo Blanco, where collecting of Nerita is not allowed, had the largest snails, the
highest density of snails, and the greatest snail biomass per unit area. Comparisons with
sites outside the reserve suggest that harvesting of unprotected populations has led to
measurable demographic effects, and that protection of this species within Cabo Blanco
has been effective.
ACKNOWLEDGEMENTS
We are grateful to Phillip Schotte, who kindly carried out the followup field sampling,
density counts, and weighing of Nerita in Cabo Blanco in September 2012. Diana
Lieberman provided statistical advice and editorial suggestions. Support for this research
was provided through the Chancellor’s office of the California State University, NSF
grant HRD0802628 from the LSAMP Program, and CSU-Monterey Bay’s Division of
Science & Environmental Policy through SEP.org.
72
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CORTES, J. & WEHRTMANN, I.S. 2009. Diversity of marine habitats of the Caribbean
and Pacific of Cost Rica. Pp. 1-45 in Wehrtmann, I.S. & Cortes, J. (Eds.), Marine
biodiversity of Costa Rica, Central America. Monographiae Biologicae Volume 86.
Springer, Berlin, Germany.
GARRITY, S. D. 1984. Some adaptations of gastropods to physical stress on a tropical
rocky shore. Ecology 65: 559-574.
GREIG-SMITH, P. 1984. Quantitative plant ecology. 3rd edition. University of
California Press, Berkeley, CA.
HURTADO, L.A., FREY, M., GAUBE, P., PFEILER, E. & MARKOW, T.A. 2007.
Geographical subdivision, demographic history and gene flow in two sympatric species of
intertidal snails, Nerita scabricosta and Nerita funiculata, from the tropical eastern
Pacific. Marine Biology DOI 10.1007/s00227-007-0620-5.
KEEN, M.A. 1971. Sea shells of tropical west America. 2nd edition. Stanford University
Press, Stanford, California.
MACGINITIE, G.E. & MACGINITIE, N. 1949. Natural history of marine animals.
McGraw-Hill Book Company, Inc. New York, NY.
MENA AGUILAR, L.A. 1995. Inventario de invertebrados de la zona de entremareas
de la Reserva Natural Absoluta de Cabo Blanco, Peninsula d Nicoya, Costa Rica.
Ministerio de Recursos Naturales, Energia Y Minas (MIRENEM), San Jose, Costa Rica.
MORRIS, R.H., ABBOTT, D.P. & HADERLIE, E.C. 1980. Intertidal invertebrates of
California. Stanford University Press, Stanford, CA.
ORTEGA, S. 1987. The effect of human predation on the size distribution of Siphonaria
gigas (Mollusca: Pulmonata) on the Pacific coast of Costa Rica. Veliger 29: 251-255.
PAINE, R.T. 1969. The Pisaster-Tegula interaction: Prey patches, predator food
preference, and intertidal community structure. Ecology 50: 950-961.
POMBO, O.A. & ESCOFET, A. 1996. Effect of exploitation on the limpet Lottia
gigantea: a field study in Baja California (Mexico) and California (USA). Pacific
Science 50: 393-403.
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RICKETTS, E.F., CALVIN, J. & HEDGPETH, J.W. 1985. Between Pacific tides. 5th
edition. Stanford University Press, Stanford, CA.
ROSENBERG, G. 2012. Nerita scabricosta Lamarck, 1822. Accessed through: World
Register of Marine Species (WoRMS) at
http://www.marinespecies.org/authority/aphia.php?p=taxdetails&id=575248 on 2012-12-
27.
SAGARIN, R.D., AMBROSE, R.F., BECKER, B.J., ENGLE, J.M., KIDO, J., LEE, S.F.,
MINER, C.M., MURRAY, S.N., RAIMONDI, P.T., RICHARDS, D. & ROE, C. 2007.
Ecological impacts on the limpet Lottia gigantea populations: human pressure over a
broad scale on island and mainland interidal zones. Marine Biology 150: 399-413.
SINAC-MINAE 2006. El sistema de áreas silvestres protegidas de Costa Rica. Report
prepared for presentation at the II Congreso Mesoamericano de Áreas Protegidas, Panamá
City, 24-26 April 2006. Ministerio del Ambiente y Energia, San Jose, Costa Rica, 96 pp.
TIMM, R.M., LIEBERMAN, D., LIEBERMAN, M. & McCLEARN, D. 2009.
Mammals of Cabo Blanco: history, diversity, and conservation after 45 years of regrowth
of a Costa Rican dry forest. Forest Ecology & Management 258: 997-1013.
WEHRTMANN, I.S. & CORTES, J. (Eds.) 2009. Marine biodiversity of Costa Rica,
Central America. Monographiae Biologicae Volume 86. Springer, Berlin, Germany.
74
Table 1. Biomass (g / m2) of Nerita snails at three sampling sites with increasing access to
harvesting. Values shown for snails on uplifted vertical rock faces and on low-lying horizontal
surfaces .
Habitat
Vertical Horizontal
Site
Cabo Blanco 80.98 g 26.75 g
Playa Los Suecos 31.89 g 52.67 g
Los Banquillos 54.41 g 27.60 g
Table 2. Analysis of weight loss over time in air-dried live Nerita snails and air-dried dead snail
tissue. Half-life refers to the length of time necessary for 50% of the initial weight to be lost.
Weight class Half-life (days), live
snails
Half-life (days), dead snail
tissue
≤ 4 g Too small to measure Too small to measure
5-9 g 25.22 2.30
10-14 g 22.51 2.55
15-19 g 20.21 2.40
≥ 20 g 23.18 2.40
Figure 1. Empty shell of the tooth shell Nerita scabricosta.
75
Figure 2. Map of study area showing three sampling sites. From the most strictly protected to
the most accessible to the public, the sites are San Miguel Biological Station, Cabo Blanco
Absolute Reserve (dark rectangle shows location of station facilities); Playa Los Suecos, at the
northern end of Reserva Cueva los Murcielagos; and Los Banquillos, on the Malpaís shore. At
each site, both horizontal and vertical habitats were sampled. Scale: 1 square = 1 km.
76
Figure 3. Collection of Nerita samples in Cabo Blanco with a 0.25 m2 quadrat. Snails were
bagged and brought to the laboratory for counting, measuring, and weighing before being
returned to the field.
(a) (b)
Figure 4. Comparison of quadrat samples (0.25 m2) taken during midday and early evening low
tides on horizontal substrates in Cabo Blanco. (a) Daytime low tide, under hot conditions; Nerita
snails were inactive, avoiding contact with the hot rock surface and sheltering in moist crevices
and under the shade of ledges; (b) early evening low tide, when conditions were cool; snails were
active, moving about over rock surfaces and grazing on algae.
77
Figure 5. Marked Nerita snails in holding aquarium prior to start of water loss trials. Nail polish
color (white, blue, green, orange, pink) indicates weight class.
Figure 6. Nerita snail with string attached to shell in preparation for weight loss experiments.
The muscular foot of the snail is clearly visible; the operculum (just to the right of the foot) is
open.
78
Figure 7. Snail density (number of individuals per m
2) in the three sample sites and the two
habitats within each site; samples taken during daytime low tides when snails were inactive.
Sample sites are ranked in terms of accessibility by the public, from Cabo Blanco (lowest
accessibility) to Los Banquillos (highest accessibility).
0
5
10
15
20
25
30
35
40
Snai
l den
sity
(n
o./
m2)
Sample site
vertical
horizontal
Cabo Blanco Los Suecos Los Banquillos
79
Figure 8. Frequency distribution of snail density (number of individuals per 0.25 m2 quadrat) in
Cabo Blanco on horizontal habitats during an evening low tide when snails had emerged from
shelter and were actively grazing. Mean density was 19.5 individuals per quadrat, or 78/m2.
0
2
4
6
8
10
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Nu
mb
er o
f q
uad
rats
Number of individuals
80
0
50
100
150
200
0.1 0.3 0.5 0.7 0.9 1.1 1.3 1.5 1.7 1.9 2.1 2.3 2.5 2.7 2.9 3.1 3.3 3.5 3.7 3.9
Freq
uen
cy
Shell diameter (cm)
(a) Cabo Blanco, vertical
0
50
100
150
200
0.1 0.3 0.5 0.7 0.9 1.1 1.3 1.5 1.7 1.9 2.1 2.3 2.5 2.7 2.9 3.1 3.3 3.5 3.7 3.9
Freq
uen
cy
Shell diameter (cm)
(b) Los Suecos, vertical
0
50
100
150
200
0.1 0.3 0.5 0.7 0.9 1.1 1.3 1.5 1.7 1.9 2.1 2.3 2.5 2.7 2.9 3.1 3.3 3.5 3.7 3.9
Fre
qu
en
cy
Shell diameter (cm)
(c) Los Banquillos, vertical
81
Figure 9. Diameter distribution of Nerita shells from three sampling sites and two habitats
within each site. (a), (b), (c), vertical habitats at Cabo Blanco, Los Suecos, and Los Banquillos;
(d), (e), (f), horizontal habitats at the same three sites.
0
50
100
150
200
0.1 0.3 0.5 0.7 0.9 1.1 1.3 1.5 1.7 1.9 2.1 2.3 2.5 2.7 2.9 3.1 3.3 3.5 3.7 3.9
Freq
uen
cy
Shell diameter (cm)
(d) Cabo Blanco, horizontal
0
50
100
150
200
0.1 0.3 0.5 0.7 0.9 1.1 1.3 1.5 1.7 1.9 2.1 2.3 2.5 2.7 2.9 3.1 3.3 3.5 3.7 3.9
Fre
qu
en
cy
Shell diameter (cm)
(e) Los Suecos, horizontal
0
50
100
150
200
0.1 0.3 0.5 0.7 0.9 1.1 1.3 1.5 1.7 1.9 2.1 2.3 2.5 2.7 2.9 3.1 3.3 3.5 3.7 3.9
Fre
qu
en
cy
Shell diameter (cm)
(f) Los Banquillos, horizontal
82
0
2
4
6
8
10
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 7.000 F 13.297 P<0.001
0
2
4
6
8
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 7.208 F 3.167 P<0.005
0
2
4
6
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 8.045 F 3.748, P<0.001
0
2
4
6
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 8.056 F 2.596 P<0.025
0246
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 8.308 F 2.890, P<0.005
0
2
4
6
8
10
12
14
16
18
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 8.980 F 8.061, P<0.001
83
02468
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 9.000 F 4.221, P<0.001
0
2
4
6
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 9.043 F 3.132, P<0.005
0
2
4
6
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 9.421 F 2.899, P<0.01
02468
10
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 9.941 F 1.315, .1<P<0.25, ns
02468
10
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 10.579 F 5.348, P<0.001
0
2
4
6
8
10
12
14
16
18
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 10.800 F 2.873, P0.001
84
Figure 10. Diameter distributions (mm) of Nerita snails sampled during a period of inactivity.
Quadrat samples (a)- (q) have been ordered from smallest to largest mean diameter. All quadrats
with at least 17 individuals are included.
0
2
4
6
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 11.111 F 2.346, P<0.025
0
2
4
6
8
10
12
14
16
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 11.400 F 5.528, P<0.001
0
2
4
6
8
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 11.429 F 3.663, P<0.001
02468
1012141618
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 12.176 F 5.049, P<0.001
0
2
4
6
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 17.514 F 0.271, P>0.75, ns
85
Figure 11. Diameter distribution (mm) of Nerita snails from the 17 individual quadrat samples
above, taken while snails were inactive.
0
20
40
60
80
100
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
17 bags pooled, mean
10.353,
var 12.664, n=498
86
0
2
4
6
8
10
12
14
16
18
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 7.596 F 5.662, P<0.001
0
2
4
6
8
10
12
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 7.718 F 3.565, P<0.001
0
2
4
6
8
10
12
14
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 8.031 F 4.223, P<0.001
0
2
4
6
8
10
12
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 8.690 7.216, P<0.001
02468
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 8.974 F 2.867, P<0.001
87
02468
10
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 9.143 F 5.327, P<0.001
0
2
4
6
8
10
12
14
16
18
20
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 9.200 F 4.464, P<0.001
02468
10
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 9.321 F 4.982, P<0.001
0
2
4
6
8
10
12
14
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 9.897 F 7.496, P<0.001
0
2
4
6
8
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 9.926 F 2.807, P<0.005
88
0
2
4
6
8
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 10.053 F 5.982, P<0.001
0
2
4
6
8
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 10.529 F 3.817, P< 0.005
02468
1012141618202224
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 10.632 F 3.555, P<0.001
02468
10
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 10.833 F 6.568, P<0.001
0
2
4
6
8
10
12
14
16
18
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 10.964 F 1.816, P<0.025
89
0
2
4
6
8
10
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 11.333 F 0.727, P>0.75, ns
0246
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 11.700 F 5.825, P<0.001
0
2
4
6
8
10
12
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 11.759 F 4.942, P<0.001
02468
1012141618202224
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 12.014 F 8.158, P<0.001
0
2
4
6
8
10
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 12.317 F 3.341, P<0.001
90
Figure 12. Diameter distributions (mm) of Nerita snails sampled during a period of feeding
activity. Quadrat samples (a) – (w) have been ordered from smallest to largest mean diameter.
All quadrats with at least 17 individuals are included.
02468
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 14.889 F 0.268, P>0.75, ns
0
2
4
6
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 17.389 F 0.306, P>0.75, ns
0
2
4
6
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
mean 19.706 F 0.208, P>0.75, ns
91
Figure 13. Diameter distribution (mm) of Nerita snails from the 23 individual quadrat samples
above, taken while snails were actively grazing.
0
20
40
60
80
100
120
140
160
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
total 23 bags, mean 10.621, var 12.938, n=804
92
Figure 14. Relationship between diameter of the Nerita shell (measured across the widest
portion) and biomass (dry weight, grams) of the snail tissue. There is an exponential relationship
(r=0.945, 27 d.f.; P<0.001), which is described by the regression equation y = 0.066e1.408x
.
Figure 15. Relationship between the mass of live, intact Nerita snails (shell plus soft tissue) and
the mass of water ejected as a response to handling. There is a positive correlation; larger snails
release larger quantities of water (r=0.909, 48 d.f.; P<0.001). The regression equation is y =
0.083x + 0.062.
0
2
4
6
8
10
12
14
0.00 0.50 1.00 1.50 2.00 2.50 3.00 3.50 4.00
Bio
mas
s (g
)
Diameter (cm )
0.0
0.5
1.0
1.5
2.0
2.5
3.0
0 5 10 15 20 25 30
Mas
s o
f w
ate
r e
ject
ed
(g)
Mass of snail (g)
93
Figure 16. Weight loss over time in samples of live air-dried Nerita snails belonging to five size
classes. The vertical axis (weight/ initial weight) is logarithmic. The regression slopes do not
vary with snail size.
y = -0.001x + 0.922 r = -0.690, 228 d.f.; P<0.01
0.1
1
0 100 200 300 400
(a) ≤ 4 g
y = -0.001x + 0.923 r = -0.622, 228 d.f.; P<0.01
0.1
1
0 100 200 300 400
(b) 5-9 g
y = -0.001x + 0.932 r = -0.752, 238 d.f.; P<0.01
0.1
1
0 100 200 300 400
(c) 10-14 g
y = -0.001x + 0.937 r = -0.759, 230 d.f.; P<0.01
0.1
1
0 100 200 300 400
(d) 15-19 g
y = -0.001x + 0.945 r = -0.850, 228 d.f.; P<0.01
0.1
1
0 100 200 300 400
Log
(wei
ght/
init
ial w
eig
ht)
Time (hours)
(e) ≥ 20 g
94
Figure 17. Weight loss over time for air-dried samples of Nerita snail tissue extracted from snails
belonging to five size classes. The vertical axis (weight/initial weight) is logarithmic. The
regression slopes are similar for all size classes.
y = -0.005x + 0.914 r= -0.825, 68 d.f.; P<0.01
0.1
1
0 100 200 300 400
(a) ≤ 4 g
y = -0.007x + 0.870 r = -0.871, 68 d.f.; P<0.01
0.1
1
0 100 200 300 400
(b) 5-9 g
y = -0.007x + 0.911 r = -0.927, 61 d.f.; P<0.01
0.1
1
0 100 200 300 400
(c) 10-14 g
y = -0.007x + 0.925 r = -0.938, 68 d.f.; P<0.01
0.1
1
0 100 200 300 400
(d) 15-19 g
y = -0.007x + 0.9253 r= -0.942, 65 d.f.; P<0.01
0.1
1
0 100 200 300 400
Log
(we
igh
t/In
itia
l we
igh
t)
Time (hours)
(e) ≥ 20 g
95
Habitat preference of the intertidal Frillfin Bathygobius (Gobiidae) in
Cabo Blanco Absolute Reserve, Costa Rica
JACOB BARRETT1, NATHANIEL BELL
2, DANIELLE KUPERUS
3, KATHLEEN SOWUL
4
1Department of Chemistry, Sonoma State University, Sonoma, CA 94928
2 Department of Biology, California State University, Sacramento, CA 95826
3Department of Biosciences, Minnesota State University -Moorhead, Moorhead, MN 56560
4Division of Science and Environmental Policy, California State University Monterey Bay,
Seaside, CA 93955
ABSTRACT. Tidepools were sampled within the rocky intertidal zone of San Miguel Biological
Station, Cabo Blanco Absolute Reserve, on the Pacific Coast of Costa Rica. Sampling was done
during six low tides between 23 June-28 June 2012. One hundred sixty fish traps, baited and
unbaited, were distributed at random among tidepools. Dimensions of each tidepool (LxWxD)
were recorded and paired readings (start and end of low tide) were made of salinity and
temperature at each trap site.
Daytime temperatures were higher than nighttime temperatures; values during the day ranged
from 30.5-42.0°C (mean 35.9°C) and nighttime temperatures from 25.0-29.0°C (mean 27.2°C).
Daytime temperatures were stable within low tide sampling periods, but nighttime temperatures
dropped during sampling periods. Daytime salinity values (range 10.0-33.5‰, mean 29.8‰)
were also higher than nighttime values (range 12.5-33.0‰, mean 27.8‰). Salinity values
remained stable from early to late low tide readings, both during daytime and nighttime
sampling.
Of the 160 traps set, a total of 31 traps (19.4%) were successful. Some traps caught more than a
single individual, and a total of 58 fish were captured. All were Frillfins (Bathygobius spp.:
Gobiidae). Trap returns were higher during the day (24/82 traps set, or 29%) than at night (7/78
traps set, or 9%). The use of bait (sausage) had no effect on rate of capture.
Bathygobius in this study were found to occupy the available tidepools at random with respect to
depth and temperature. Fish responded to salinity, however; those caught in nighttime samples
showed a preference for low salinity levels, and those during the day were most often found in
tidepools with moderate and stable mean values of salinity.
96
INTRODUCTION
Gobies are the largest family of fish in the tropical Eastern Pacific with approximately 80 species
and are the largest family of marine fishes in the world with around 220 genera and 1600 species
(Allen & Robertson 1994). Due to their high abundance, gobies are an important part of the food
chain in marine, estuarine and freshwater habitats. Typically 10 cm or less in length, gobies are
usually found on sand, silt, or mud bottoms (Allen & Robertson 1994).
The frillfin genus Bathygobius Bleeker 1878 has a circumtropical distribution, where it is found
primarily in nearshore, littoral habitats (Miller & Stefanni 2001) Cabo Blanco is within the
geographical ranges of two species of intertidal frillfins, Bathygobius ramosus Ginsburg 1947
(found from Baja California to Peru) and Bathygobius andrei (Sauvage 1880) (found from Costa
Rica to Ecuador).
The San Miguel (western) sector of the Cabo Blanco reserve includes extensive areas of
tidepools and rocky reefs, a sheltered inshore lagoon with close to 100 species of reef fish, and
wave-exposed and sheltered sand and cobble beaches. Tides are semi-diurnal. Tidal amplitude
(vertical difference between high and low tide) is as much as 3.05 m. Because the intertidal area
is generally level in profile, the rocky area exposed at low tide is extensive.
Here we evaluate captures of frillfins in fish traps in San Miguel in relation to time of day
(daytime and nighttime low tides) and tidepool conditions (tidepool area and depth, water
temperature, and salinity).
METHODS
Field sampling took place from 23-28 June 2012 at low tide. Traps were placed in tidepools on
the rocky intertidal platform in front of the San Miguel Biological Station. Sampling times are
shown with respect to tidal cycles and time of day in Figure 1.
Fish traps were made from translucent plastic soda bottles, as shown in Figure 2. Approximately
half of the traps, randomly selected, were baited with sausage meat cut into cubes; the remaining
traps were placed without bait.
Four investigators were in the field during the collection times (three days and three nights).
Sampling began around 1 hour before low tide. Tidepools were chosen according to a stratified
random design on each sampling occasion. From an arbitrary starting point, the investigators
walked over the rocky area taking tidepools in the order they were encountered. Only tidepools
deep enough to completely cover a submerged trap were included. Areas in the lowest part of the
subtidal were excluded if they were likely to be covered by the rising tide before the trap could
be retrieved.
The sampling protocol once a tidepool was selected was as follows: (1) Water temperature was
measured and the time recorded; (2) a small sample of water was collected in a clean vial for
salinity testing; (3) the depth, length, and width of the tidepool were measured; (4) the fish trap
(baited or unbaited) was submerged; and (5) GPS coordinates at the site of the trap were noted.
97
Approximately 30 minutes after low tide, the investigators began to re-visit each tidepool to
collect traps. The protocol was as follows: (1) the trap was picked up for return to the laboratory;
(2) a second temperature reading was taken and the time recorded; (3) a second water sample
was collected for salinity testing; and (4) fish traps were returned to the laboratory and captured
fish transferred into aquaria.
All captured fish were photographed, measured, and weighed in the laboratory.
Salinity was tested in the laboratory using a VEEGEE model A366 ATC salinity refractometer,
calibrated and rinsed with deionized water. Temperatures were taken with an Enviro-Safe USA
0-50°C thermometer with an accuracy of ±0.5°C.
All fish were measured, weighed and photographed. Fish specimens to be preserved were placed
in formaldehyde for one week, transferred to water for one day, and then moved to 75% ethanol.
RESULTS
Physical Environment
During the period of the study, air temperatures ranged from 20°C to 27°C. Rain fell once, on
the night of 26 June, producing 4 mm of rain. Cloud cover was from 20% to 30%.
The tidepools which were sampled (both day and night) ranged in depth from 0.06 m to 0.42 m
with a mean depth of 0.18 m.
Area estimates of the sampled tidepools ranged from 0.09 m2 to 300 m
2, with a mean area of
30.4 m2.
Daytime water temperatures in tidepools ranged from 30.5°C to 42.0°C. Daily maximum air
temperature during the same period was constant during the study period at 27°C.
A paired t-test comparing the two temperature readings for each tidepool in the daytime samples
showed no difference between the initial and final temperatures (t=1.440, 80 d.f.; P>0.05).
Averaged temperatures for each tidepool were used for subsequent data analysis. The averaged
temperatures had a range of 33.3°C to 41.0°C with an overall mean of 35.9°C.
Nighttime temperatures in tidepools ranged from 25.0°C to 29.0°C. Daily minimum air
temperature during the same period was constant during this period at 20°C.
A paired t-test comparing the two temperature readings for each tidepool sampled at night
showed that initial temperatures decreased during the period between measurements (t=11.320,
77 d.f.; P<0.05). The averaged temperatures had a range of 26.0°C to 28.3°C with a an overall
mean of 27.2°C.
98
Daytime absolute lowest value of salinity was 9.0‰, and the absolute highest was 35.0‰. A
paired t-test (initial vs. final salinity readings for each tidepool) showed no difference between
the initial and final salinities (t=0.549, 72 d.f.; P>0.05), hence averaged daytime salinity values
for each tidepool were used for data analysis and plotting of frequency distributions. The
minimum daytime salinity (of the averaged values) was 10.0‰ and the maximum was 33.5‰,
with a mean of 29.8‰.
Nighttime absolute lowest value of salinity was 10.0‰ and absolute highest value was 35.0‰.
A paired t-test (initial and final salinity readings for each tidepool) showed no difference
between the initial and final salinities (t=0.586, 76 d.f.; P>0.05), and the average averaged
nighttime salinities were therefore used for data analysis and frequency distributions. The
minimum nighttime salinity (of the averaged values) was 12.5‰ and the maximum was 33.0‰,
with a mean of 27.8‰.
Daytime and nighttime readings differed for temperature (cooler at night; t=57.19, 157 d.f.;
P<0.05) and for salinity (lower at night; t=3.251, 148 d.f.; P<0.05).
Fish Captures
GPS coordinates of sampled tidepools, with and without fish captures, are mapped in Figure 3.
All 58 specimens captured were frillfins belonging to the genus Bathygobius (family Gobiidae).
Multiple fish, from 2-7 individuals, were sometimes captured in a single trap.
Total fish length ranged from 3.7 cm to 8.6 cm with a mean of 5.6 cm. Fish weight ranged from
0.5 g to 7.5 g with a mean of 2.3 g. There was an exponential relationship between fish length
and fish weight (r=0.934, 56 d.f.; P< 0.001) (Figure 4).
Traps set during the day captured more fish than traps set at night (Table 1), based on a test of
association (G=11.070, 1 d.f.; P<0.05).
Capture of fish was independent of the presence or absence of sausage bait (G=0.830, 1 d.f.;
P>0.05) (Table 2). Sausage as bait did not make the traps more effective at capturing fish.
Testing for habitat preference
In order to test whether or not Bathygobius fish show a preference for certain tidepool conditions
or whether they occupy tidepools at random with respect to any given tidepool variable, we
compared tidepools in which fish were captured with tidepools in which no fish were caught.
Variables tested included temperature (daytime and nighttime),
Student’s t tests were used to compare mean values of a given variable, testing whether fish
showed a preference for high or low values of a given variable. Further, F tests were used to
assess whether the variance of a given variable differed between the two groups of tidepools,
thus testing whether or not fish occupied a narrow, restricted subset of available conditions and
avoided the extremes at both ends of the distribution.
99
Habitat preference: temperature
During daytime sampling, tidepools in which fish were not captured ranged in temperature from
33.5°C to 41.0°C with a mean of 35.98°C. Those in which fish were caught ranged in
temperature from 34.0-38.5°C with a mean of 35.58°C. The daytime temperatures of tidepools
with fish and without fish did not differ (t=1.430, 80 d.f.; P>0.05). Likewise, the variances of
the temperatures for traps with and without fish did not differ (F=1.69, ν1=57, ν2=23; P>0.05).
At night, tidepools without captured fish ranged in temperature from 26.0°C to 28.3°C with a
mean of 27.18°C. Those in which fish were trapped ranged in temperature from 26.5-28°C with
a mean of 27.07°C. The nighttime temperatures of tidepools with fish and tidepools without fish
did not differ (t=0.480, 76 d.f.; P>0.05). Further, the variances of the temperatures for traps
containing fish and traps lacking fish did not differ (F=1.28, ν1=6, ν2=70; P>0.05).
The difference between initial and final temperatures (ΔT) may be considered a measure of
short-term temperature stability within the tidepool, over the period of a given low tide. For
daytime samples the maximum difference between initial and final temperatures (ΔT) for
tidepools without fish captures was 6°C, with a mean ΔT of 1.70°C. The maximum ΔT for
tidepools with trapped fish was 4°C, with a mean Δ T of 1.70°C. Daytime ΔT for tidepools with
fish and without captured fish were not different, (t=0.020, 78 d.f.; P>0.05), nor were the
variances of ΔT for traps with fish and without fish (F=1.54, ν1=56, ν2=22; P>0.05).
For the daytime samples the largest negative change in temperature was -6°C and the largest
positive change in temperature was 5°C. The mean change in temperature between initial and
final temperatures within a tidepool was 0.35°C.
For nighttime samples the maximum ΔT for tidepools without captured fish was 2.5°C, with a
mean of 0.81°C. The maximum ΔT for tidepools in which fish were captured was 2.0°C with a
mean of 1.00°C. Nighttime ΔT for tidepools with and without fish caught did not differ (t=0.74,
75 d.f.; P>0.05). Similarly, the variance of ΔT for traps with fish and without fish did not differ
(F=1.73, ν1=69, ν2=6; P>0.05).
For the nighttime samples the largest negative change in temperature was -2.5°C and the largest
positive change in temperature was 1.5°C with a mean of -0.78 °C.
Based on these results, Bathygobius fish in this area showed no habitat preference with respect to
tidepool temperature or stability of tidepool temperature in either the daytime or nighttime
samples, nor did they occupy tidepools with a narrow range of temperatures.
Habitat preference: salinity
For samples done during daytime low tides, tidepools with traps not containing fish ranged in
salinity from 10.0-33.5‰ with a mean of 29.04‰. Tidepools that contained fish ranged in
salinity from 20.0-33.0‰ with a mean of 30.40‰. The daytime salinity for tidepools containing
fish and lacking fish did not differ (t=1.730, 80 d.f.; P>0.05). However, the variance in salinity
for traps containing fish was lower than that for those without fish, (F=3.69, ν1=57, ν2=23;
P<0.05). Thus, for daytime samples, while the mean salinity level was equivalent for both
groups of tidepools, fish occurred in tidepools with a restricted or narrow range of salinity.
100
For nighttime samples, traps not containing fish ranged in salinity from 12.5-33.0‰ with a mean
of 27.89‰. The nighttime range of salinity for traps containing fish was 14.0-31.0‰ with a
mean of 22.86‰. During the nighttime, salinity in tidepools with fish was lower than that in
tidepools without fish (t=2.46, 76 d.f.; P<0.05). Variance in salinity, on the other hand, was
found not to differ between traps with and without fish (F=1.25, ν1=6, ν2=70; P>0.05). At night,
therefore, fish were found in tidepools with lower salinities, on average, but did not occupy a
reduced range of salinities.
The difference between initial and final salinity values (ΔS) is a measure of short-term stability
in salinity conditions within a tidepool. During the daytime the maximum value of ΔS for
tidepools without fish was 9.0‰, with a mean of 1.74‰. The maximum ΔS for tidepools with
fish was 5.0‰, with a mean of 1.09‰. The mean ΔS of tidepools containing fish and lacking
fish did not differ (t=1.79, 71 d.f.; P>0.05). However the variance of ΔS for tidepools with fish
was lower than that of pools lacking fish, (F=2.17, ν1=49, ν2=22; P<0.05). Thus, for daytime
samples, while the mean ΔS was equivalent for tidepools with and without captured fish, the fish
were more likely to be captured in tidepools with a lower range of ΔS, that is, in tidepools with
more consistent short-term stability in salinity levels.
For daytime samples the largest negative change in salinity was -5‰ and the largest positive
change in salinity was 9‰ with a mean of -0.3‰.
For nighttime samples, the maximum ΔS for tidepools without fish was 15.0‰ with a mean of
2.59‰ and the maximum ΔS for tidepools containing fish was 13.0‰ with a mean of 4.00‰.
The mean ΔS for tidepools with and without fish did not differ (t=0.770, 75 d.f.; P>0.05), nor did
the variance of ΔS for tidepools with and without fish, (F=1.83, ν1=69, ν2=6; P>0.05).
For nighttime samples the largest negative change in salinity was -15‰ and the largest positive
change in salinity was 10‰, with a mean of -1.3‰.
Habitat preference: tidepool area and depth
Fish captures with respect to tidepool depth were analyzed separately for daytime and nighttime
sample periods. Tidepools without fish captures during the day ranged in depth from 0.06 m -
0.42 m (mean=0.180 m). Those with captured fish ranged from 0.10 m – 0.37 m (mean=0.162
m). Mean tidepool depths for pools with captured fish and pools without fish during the day were
not different (t=1.08, 80 d.f.; P>0.05), nor did their variances differ (F=1.82, ν1=57, ν2=23,
P>0.05).
Tidepools without fish captures during the night ranged in depth from 0.06 m – 0.40 m
(mean=0.176 m). Those with captured fish ranged from 0.15 m – 0.24 m (mean=0.180). Mean
tidepool depths for pools with captured fish and pools without fish (nighttime samples) were not
different (t=0.25, 76 d.f; P>0.05), nor were the variances different (F=3.56, ν1=70, ν2=6,
P>0.05). Fish were distributed at random with respect to tidepool depth, both during the day and
at night.
101
Fish size was independent of the depth of the tidepools in which they were caught. This lack of
correlation was found both for fish length (Figure 13; r=0.148, 56 d.f.; P>0.05); and fish weight
(Figure 14; r=0.045, 56 d.f.; P>0.05).
DISCUSSION
All of the fish caught belong to the genus Bathygobius (family Gobiidae). Based on
morphological characteristics, especially color pattern, we identified 31 of the captured
specimens as B. ramosus (Panamic frillfin). The remaining 27 specimens may belong to either B.
ramosus or the nearly identical B. andrei (Estuary frillfin), and their identification remains
uncertain. Definitive separation of these two species may depend upon molecular genetic
information (Miller & Stefanni 2001). Because of difficulties in the separation of the two
species, analyses in this study were completed at the level of genus.
Clearly the traps were highly effective in catching frillfins. Since these fish tend to cling to or
bury themselves in substrate, they may have been unable, once they entered the trap, to exit the
trap via the narrow mouth which was elevated above the bottom of trap. Other species of fish
which were observed in the tidepools were not caught; we do not know if they never entered the
trap, or if they entered the trap and were subsequently able to escape.
The use of sausage as bait did not affect the success rate of Bathygobius traps. Although minced
sausage releases a strong scent, the results suggest that Bathygobius was neither attracted nor
repelled by the bait. Why the frillfins entered the traps is unknown; they may have done so in
search of protection or by accident.
Although they were the only fish captured, Bathygobius were not the only species observed in
the tidepools. During the day, Signal Triplefins (Lepidonectes clarkhubbsi) and juveniles of the
Acapulco Gregory (Stegastes acapulcoensis) were observed. A large number of additional
species were seen at night, including Mullet (Mugil sp.), Guineafowl Puffer (Arothron
meleagris), Elegant Clingfish (Arcos decoris) Panamanian Sergeant (Abudefduf troschelii), and
the Panamic Nightsergeant (Abudefduf concolor). Invertebrates noted during the sampling
include octopus.
Fewer frillfins were captured at night in this study than during the day. This could reflect a
behavioral rhythm, in which the fish tend to be more active during the day. Alternatively, the
higher density of other fish in the tidepools at night may have inhibited the activity level of
Bathygobius and could thus have affected trap returns.
Bathygobius in our samples occupied tidepools at random with respect to temperature, showing
no selectivity for temperature conditions either during daytime nor nighttime sample periods.
Preference was shown, however, with respect to salinity. During daytime low tides, fish tended
occur within a restricted range of salinities, avoiding either extreme, while at night, they
preferred tidepools with comparatively low salinity levels.
102
It is interesting that these fish were caught in tidepools with a narrow range of salinities and
comparatively stable salinity levels. Bathygobius and other tidepool fishes differ from “open-
water” fishes in that their habitat undergoes extreme changes in temperature and salinity; with
every tidal cycle they are alternately submerged in seawater up to 3 m in depth and isolated in
small pools where they are exposed to the elements. Although this species lives in a unstable and
highly variable environment, they nonetheless appear to seek out areas of little to no change in
salinity.
Bathygobius have the ability move freely between tidepools. Our study indicates that they
occupy tidepools at random with respect to depth and temperature, but choose tidepools on the
basis of salinity.
ACKNOWLEDGEMENTS
We thank the staff at San Miguel Biological Station, Cabo Blanco Absolute Reserve for
logistical support. The bottle Traps were designed with the help of Milton Lieberman, Diana
Lieberman, ,and Dean Philpot. Diana Lieberman offered statistical advice and editorial
comments on the manuscript. Support for this research was provided through the Chancellor´s
Office of the California State University and NSF grant HRD-0802628 from the LSAMP
program of the National Science Foundation. Programmatic funding was made available by
CSU-Monterey Bay’s SEP.org.
LITERATURE CITED
ALLEN, G.R. & ROBERTSON, D.R. 1994. Fishes of the tropical eastern Pacific. University
of Hawaii Press, Honolulu, HI.
MILLER, P.J. & STEFANNI, S. 2001. The eastern Pacific species of Bathygobius
(Perciformes: Gobiidae). Revista de Biologia Tropical 49 (Supl. 1): 141-156.
103
Table 1. Test for association between trap success and time of day (daytime vs nighttime), based
on a total of 160 trap sets. Captures of fish were more likely to occur during daytime low tides
(G=11.070, 1 d,f,l P<0.001).
Time of day
Day Night Total
Fish captured 24 7 31
Fish not captured 58 71 129
Total 82 78 160
Table 2. Test for association between trap success and the placement of sausage bait in the
bottle trap, based on a total of 160 trap sets. Captures of fish were independent of the presence
or absence of bait (G=0.830, 1 d.f.; P>0.05).
Sausage bait
Present Absent Total
Fish captured 17 14 31
Fish not captured 59 70 129
Total 76 84 160
104
Figure 1. Tidal cycle in the study area from 22 June-28 June 2012. Sample times are indicated
(white boxes, daytime samples; black boxes, nighttime samples). The number of Bathygobius
captured at each low tide is indicated above the respective box.
Figure 2: Manufacture of fish traps using translucent plastic soda bottles, nylon string, rock, and
duct tape. The top third of bottle is cut off from the bottom two-thirds, then inverted and inserted
into the bottom portion. Two slits are cut into the bottom section through which the string is fed.
The top portion is duct taped into place, keeping the mouth of the bottle from touching the sides
of the bottle. A rock is tied to the bottle to act as an anchor. With a dissecting needle, holes are
made in the end of the bottle to aid in water flow and venting of air bubbles. (Design from D.
Lieberman & M. Lieberman, personal communication).
105
Figure 3. Map showing location (diamonds) of bottle traps set on the rocky intertidal zone at San
Miguel Biological Station. The point labeled “Eagle Rock” (square) acted as a daily reference
point. Traps that successfully caught fish are marked with an X. Mapping was done with GPS.
120
130
140
150
160
170
180
190
200
210
220
230
240
250
260
270
280
670 680 690 700 710 720 730 740 750 760 770 780
Wes
t
North
GPS (West)
Eagle Rock
Fish
106
Figure 4. Relationship between length and weight for a sample of 58 individuals of Bathygobius.
There is a exponential relationship (r = 0.934, 56 d.f.; P<0.001) defined by the regression
equation y = 0.138e0.466x
.
107
Figure 5: Depth of tidepools versus the length of fish caught. Fish length is independent of
tidepool depth (r=0.148, 56 d.f.; P>0.05).
Figure 6: Depth of tidepools versus the weight of the fish caught. Fish length is independent of
tidepool depth (r=0.005, 56 d.f.; P>0.05).
108
Comparison of biomechanical properties of hermit crabs using contrasting
shell types on a tropical shore
AMIE NOWACKI1, ADRIANNA HERNANDEZ
2, and CARLOS DE LA PARRA
3
1 Department of Biosciences, Minnesota State University – Moorhead, Moorhead, MN 56563
2Department of Biology, California State University Los Angeles, Los Angeles, CA 90032
3Department of Environmental Engineering, California Polytechnic State University, San Luis
Obispo, CA
ABSTRACT. In a study at San Miguel Biological Station, Cabo Blanco Absolute Reserve on the
Pacific Coast of Costa Rica, we compared six commonly-utilized shell types of hermit crabs in
terms of size, speed, strength, and resistance to crushing. Two hundred forty hermit crabs were
sampled. Half of the individuals were examined for hermit crab performance (size, pulling
force, velocity), and the remaining were utilized for shell physical properties (length, width,
thickness of shell, and resistance to crushing We tested turban shells (Turbo saxosus,
Turbinidae); tooth shells (Nerita scabricosta, Neritidae); rock shells (Acanthais brevidentata,
Muricidae); ceriths (Cerithium muscarum, Cerithiidae); bubble shells (Bulla punctulata,
Bullidae); and shells of an unidentified pulmonate land snail (Stylommatophora, Pulmonata).
In general, larger crabs were faster and stronger than small crabs. Results of hermit crab
trials done with the shell in place were correlated with results of trials after the crabs had been
extracted from the shell. The shell species with the best performance were tooth shells and
turban shells (size, velocity, and pulling strength). The shell species with the greatest resistance
to crushing were rock shells, turbans and ceriths. The shells chosen most frequently by hermit
crabs in this area are tooth shells, which in the current study showed the best performance.
INTRODUCTION
Tropical terrestrial hermit crabs (Coenobita compressus: Coenobitidae) are exposed to
multiple stressors from the environment, including predation (Vance 1972; Angel 2000;
Pechenik and Lewis 2000), osmotic changes, and desiccation (Bertness 1981). Their soft,
unprotected posterior segments make them particularly susceptible to these different
environmental conditions. Another group of marine animals facing these conditions sharing
many of the same predators (spiny lobsters, crabs, stomatopods, bony fish, and elasmobranchs)
are marine snails, or gastropods (LaBarbera & Merz 1992). As soft bodied mollusks, gastropods
depend for protection on shells. Hermit crabs use empty gastropod shells for protection against
predation and desiccation, but carrying shells is energetically costly (Osorno et al. 2005). We
hypothesize that hermit crabs select the shell types that offer higher performance and hence
higher chances of survival than would be had with other types of shells or with no shell at all.
109
Although some research has been done on gastropod architecture (Bertness 1981), shell
strength (LaBarbera and Merz 1992), size and type of shell preference (Osorno et al. 1998,
2005), and energy consequences of shell choice (Osorno et al. 2005), there is little information
on the biomechanical properties of hermit crabs and the benefits and costs of using certain shell
types. The present study compares commonly-utilized shell types, using a range of sizes of each,
with respect to crab speed, crab strength, and resistance of the shell to crushing, and considers
the relationship between shell species preference and biomechanical properties of the hermit
crabs and their shells.
METHODS
The study was carried out at San Miguel Biological Station, Cabo Blanco Absolute
Reserve. The reserve is located near the tip of the Nicoya Peninsula, and consists of
approximately 4,000 hectares of tropical coastal dry forest and marine habitats. The climate is
hot and humid, with a temperature range of 15 to 35⁰C. The terrestrial hermit crab Coenobita
compressus (Coenobitidae) is extremely abundant on the sandy beach and in the coastal forest
near the shore.
Six species of gastropod shells were selected for study, varying in size and morphology.
All six are species commonly used by hermit crabs in this area: turban shells (Turbo saxosus,
Turbinidae); tooth shells (Nerita scabricosta, Neritidae); rock shells (Acanthais brevidentata,
Muricidae); ceriths (Cerithium muscarum, Cerithiidae); bubble shells (Bulla punctulata,
Bullidae); and shells of an unidentified pulmonate land snail (Stylommatophora, Pulmonata)
(Figure 1). Taxonomy of the gastropod shells follows Keen (1971), updated according to
Appeltans et al. (2012).
The hermit crabs used for this experiment were collected from a compost pile 50 m from
the shore. A total of 240 hermit crabs (40 of each species) were selected. Trials with the first
120 individuals focused on hermit crab performance, and those for the remaining 120 focused on
shell morphology and physical properties. An effort was made to include a representative range
of sizes for each shell species. Trials of strength and speed were carried out first using hermit
crabs with their shells, after which the crabs were carefully removed from their shells by hand to
permit both testing of the performance of the crabs without their shell and testing of the
properties of the shells themselves.
At the outset, each hermit crab shell was individually marked with nail polish, and the
weight of the crab plus the shell was measured to the nearest 0.01 g using a Pesola spring scale.
After extraction of a hermit crab, the crab and its empty shell were weighed separately, and the
length of the left back leg was measured to the nearest 0.01 mm using a dial caliper. After the
measurements were taken and the tests were performed, the first 120 hermit crabs were released.
During the three days and two nights spent in the laboratory they were kept in plastic bins with a
considerable amount of leaf litter and were fed fresh coconut meat each night from the trees
along the coast.
110
A total of 120 hermit crabs were tested for strength, first with shells, and then without
shells (Figure 2a and 2b). The pulling force (lbf) was measured using an IMADA D12 Digital
Force Gauge. A nylon string of negligible weight was used to connect the crab to the gauge; one
end of the string was connected to the gauge with a loop, and the other was attached to the top of
the shell with duct tape. A corridor measuring 5 x 15 x 7 cm was set up on a laboratory table for
the force track. A 5 x 15 cm piece of tree bark provided traction and presented a more realistic
surface for the hermit crabs to walk upon. The highest measurement of force registered in a trial
period of 15 seconds was recorded.
The same protocol was followed for the pulling trials of hermit crabs without shells,
except that the harness with a slip knot was secured between the two last pairs of legs on either
side of the hermit crab in order to connect the bare hermit crab to the force gauge.
A total of 120 hermit crabs were tested for speed, first with shells and later without. The
velocity trials were carried out on a rectangular track measuring 60 x 250 x 9 cm laid out in a
clearing in the forest approximately 25 m from the shore. The area was raked free of leaf litter
until the dark, slightly moist soil was exposed. The track area was delimited by low wooden
walls and a line was drawn to designate a starting point. At the time the trials were performed,
the air temperature was 28°C, relative humidity was 97%, and wind speed was very light at 1.2
kph.
Hermit crabs were placed individually at the starting line. Once the crab had begun to
move and reached a constant velocity, a stopwatch was used to measure a 15 second trial period.
During the run, the path followed by the crab was marked by inscribing a line in the soil with a
sharp stick. A piece of string laid in the crab’s track was then measured in length with a meter
stick to obtain the distance traveled in the allotted 15-second period.
Hermit crabs which had been extracted from their shells were transported from the
laboratory to the velocity track in plastic Dixie cups; each cup was placed on the starting line and
tipped sideways to direct the crab to move along the track (Figure 3).
Empty shells were tested for resistance to crushing by applying weight to the shell until
the point of failure, when the shells shattered. Two flat rocks acting as clamps were placed on
the center of a bathroom scale (280 lb maximum) and the shells individually placed in between
the rocks. An investigator stepped on the rock, applying pressure from above with the foot. The
shells were placed with the aperture facing down; care was taken to apply a vertical force, and to
avoid tilting the rocks. The highest reading on the scale was recorded just at the moment of
crushing. In the event that a chip occurred on the shell but the shell did not shatter, additional
weight was applied until the shell was completely crushed. In a very small number of shells (3-
5), a small chip broke off of the aperture or the top of the shell; the test was continued until the
shell itself shattered, and the crushing weight at that point was recorded.
A second set of 120 hermit crabs with shells belonging to the same six gastropod species
were collected from the compost pile, and the same procedure followed for shell measurement,
marking and extraction of hermit crabs.
111
The crabs were released after extraction and only the shells kept for further analysis.
Shell measurements were made to the nearest 0.01 mm using a dial caliper of length of aperture
(from head to claw cross section); width of aperture; thickness of the aperture (lip of shell);
length of shell; and width of shell. The shells were crushed in the same fashion as before, and
broken fragments of the shell were then used to obtain a measurement of the thickness of the
shell material making up the body of the shell.
RESULTS
Analyses with all six species pooled. -- Weights of hermit crabs and weights of their
shells varied extensively both within and between shell species. Based on a sample of 240
individuals, crab weight ranged from 0.03 – 14.24 g ( ̅ = 1.322 g). Shell weight ranged from
0.05 – 16.30 g ( ̅ = 1.853 g).
When all 240 individuals in all six species are considered, weight of the crab is correlated
with the weight of the shell (r = 0.516, 236 d.f. ; P<0.05). The length of the left back leg is
correlated with weight of crab both with the shell (r = 0.711, 236 d.f.; P<0.05) and without the
shell (r = 0.732, 236 d.f.; P<0.05) (Table 1). Crabs using turban shells and tooth shells were
heavier than crabs using the other species of shells; crabs using land shells, rock shells, and
ceriths were the lightest (Figures 4a and 4b).
With all six species pooled, larger crabs were faster than smaller crabs. The weight of
crabs with the shell was correlated with the velocity of crabs tested with the shell (r = 0.211, 118
d.f.; P<0.05) as well as without the shell (r = 0.415, 99 d.f.; P<0.05). Leg length was correlated
with the velocity of crabs tested with the shell (r= 0.528, 115 d.f.; P<0.05) and without the shell
(r = 0.516, 99 d.f.; P<0.05) (Table 1).
Likewise, when all species are pooled, strength was greatest in large crabs. The pulling
force of crabs tested with the shell (r = 0.641, 104 d.f.; P<0.05) and without the shell (r = 0.525,
104 d.f.; P<0.05) showed a positive correlation with the weight of the crab. The force of crabs
tested without the shell was correlated with leg length (r = 0.621, 104 d.f.; P<0.05), although the
pulling force of crabs tested with the shell was independent of leg length.
When all species are considered, the velocity of crabs tested with the shell was correlated
with their velocity when tested without the shell (r = 0.603, 99 d.f.; P<0.05). Likewise, when all
species are included, the pulling force of crabs tested with the shell was correlated with their
force when tested without the shell (r = 0.667, 104 d.f.; P<0.05) (Table 1).
When all species of shells are considered, crab velocity is correlated with pulling force,
both when tested with the shell (r = 0.497, 118 d.f.; P<0.05) and without the shell (r = 0.636, 99
d.f.; P<0.05) (Table 1).
Speed and strength of hermit crabs varied among shell species. Hermit crabs with tooth
shells are the fastest ( ̅=7.61 cm/sec) and pull with the greatest strength ( ̅=0.092 lbf); while the
hermit crabs with cerith shells are the slowest ( ̅=4.43 cm/sec) (Figures 5a and 5b) and exert the
weakest pulling force ( ̅=0.041 lbf) (Figures 6a and 6b).
112
The weight necessary to crush shells varied greatly, from 1.81-121.11 kg, with a mean of
24.12 kg. When analyzing shells of all species pooled, it was found that the weight necessary to
crush the shell was correlated with the weight of the shell (r = 0.732, 235 d.f.; P<0.05) as well as
the thickness of the shell material from the body of the shell (r = 0.514, 117 d.f.; P<0.05) (Table
2).
With all species and individuals considered, the thickness of the shell at the aperture was
correlated with the thickness of the shell body, away from the lip (r = 0.510, 117 d.f.; P<0.05)
(Table 2). Correlation between aperture of the shell and length of the shell was positive (r =
0.572, 118 d.f.; P<0.05) (Table 2). There is a positive correlation between shell width and shell
length when all species are pooled (r = 0.698, 118 d.f.; P<0.05) (Table 2).
Species of shells differed with respect to resistance to crushing. Land snail shells and
bubble shells were the easiest to crush ( ̅= 11.6 kg), while the rock shells were the most resistant
to crushing ( ̅= 32.3 kg) (Figures 7a and 7b).
Analyses within individual species -- The weight of shell shows a positive correlation
with weight of crab in tooth shells only (r = 0.604, 38 d.f.; P<0.05), but not in the other species
tested. There was a positive correlation between weight of crab and leg length, however, within
each of the six species: tooth (r = 0.812, 38 d.f.; P<0.05), rock (r = 0.591, 37 d.f.; P<0.05), cerith
(r = 0.675, 38 d.f.; P<0.05), turban (r = 0.537, 37 d.f.; P<0.05), bubble (r = 0.519, 38 d.f.;
P<0.05) and land (r = 0.520, 37 d.f.; P<0.05) (Table 3).
The relationship between crab size and speed was analyzed within each shell species.
Crab weight and crab velocity were correlated in two out of the six species: ceriths (r = 0.781, 18
d.f.; P<0.05) and land snails (r = 0.702, 18 d.f.; P<0.05). Velocity of crab versus leg length
shows a positive correlation only within ceriths (r = 0.691, 18 d.f.; P<0.05) (Table 4).
The analysis of crab weight and pulling force (lbf) showed a positive correlation for
ceriths (r = 0.748, 18 d.f.; P<0.05) and turbans (r = 0.543, 18 d.f.; P<0.05) and no others. Leg
length was correlated with pulling force in ceriths alone (r = 0.640, 15 d.f.; P<0.05) (Table 5).
Correlations between weight of crab with the shell included and performance were
analyzed within each species. The total weight of hermit crabs was positively correlated with the
left back leg length in all of the six species: tooth (r = 0.879, 38 d.f.; P<0.05); rock (r = 0.722, 37
d.f.; P<0.05); cerith (r = 0.791, 38 d.f.; P<0.05); turban (r = 0.740, 38 d.f.; P<0.05); bubble (r =
0.631, 38 d.f.; P<0.05); and land (r = 0.798, 37 d.f.; P<0.05) (Table 6).
The velocity of crabs tested with the shell was correlated with weight of the crab with its
shell in ceriths (r = 0.682, 18 d.f.; P<0.05) and bubble shells (r = 0.445, 18 d.f.; P<0.05) but not
in other species (Table 4).
113
The pulling force of crabs tested with the shell was correlated with weight of the crab
with the shell in all species except turban and land shells: tooth (r = 0.634, 18 d.f.; P<0.05);
rock (r = 0.528, 18 d.f.; P<0.05); cerith (r = 0.904, 18 d.f.; P<0.05); bubble shells (r = 0.685, 18
d.f.; P<0.05); and land snails (r= 0.598, 18 d.f.; P<0.05) (Table 5).
Correlations between speed and force were tested for individual crabs within each
species. Velocity of crabs without the shell and pulling force without the shell show a positive
correlation in tooth shells (r = 0.673, 18 d.f.; P<0.05), rock (r = 0.591, 17 d.f.; P<0.05) and
ceriths (r = 0.844, 14 d.f.; P<0.05) (Table 7). On the other hand, velocity of crab with the shell
and force of crab with the shell show a positive correlation in rock shells (r = 0.561, 17 d.f.;
P<0.05), ceriths (r = 0.731, 18 d.f.; P<0.05) and land snail shells (r = 0.450, 18 d.f.; P<0.05)
(Table 7).
Velocity of crabs with the shell and without the shell was correlated in all of the species
except bubble shells: tooth (r = 0.567, 18 d.f.; P<0.05); rock (r = 0.552, 17 d.f.; P<0.05); cerith
(r = 0.808, 14 d.f.; P<0.05); turban (r = 0.531, 16 d.f.; P<0.05); and land (r = 0.740, 8 d.f.;
P<0.05). Hermit crabs that ran the fastest while carrying their shell continued to run the fastest
after they were extracted from their shell.
Pulling force of crabs with the shell and without the shell showed a positive correlation in
tooth shells (r = 0.557, 18 d.f.; P<0.05); rock (r = 0.813, 17 d.f.; P<0.05); cerith (r = 0.893, 15
d.f.; P<0.05); and land snails (r = 0.715, 11 d.f.; P<0.05) (Table 7). Those crabs that exerted a
stronger force while carrying their shell also exerted a stronger force when extracted from their
shell.
When species were analyzed individually, shell width was correlated with shell length in
all but ceriths: tooth (r = 0.987, 18 d.f.; P<0.05); rock (r = 0.982, 18 d.f.; P<0.05); turban (r =
0.930, 18 d.f.; P<0.05); bubble (r = 0.950, 18 d.f.; P<0.05); and land (r = 0.767, 18 d.f.; P<0.05)
(Table 8). There was a positive correlation between width and length of the aperture in all six
species: tooth (r = 0.835, 18 d.f.; P<0.05); rock (r = 0.950, 18 d.f.; P<0.05); cerith (r = 0.915, 18
d.f.; P<0.05); turban (r = 0.934, 18 d.f.; P<0.05); bubble (r = 0.917, 18 d.f.; P<0.05); land (r =
0.910, 18 d.f.; P<0.05) (Table 8). Aperture thickness and shell body thickness were correlated
within tooth shells (r = 0.633, 18 d.f.; P<0.05) and ceriths (r = 0.659, 17 d.f.; P<0.05) (Table 8).
Within species, there was no correlation between resistance to crushing and weight of
shell; heavier shells were not harder to crush. Crushing weight and thickness of the shell body
were correlated in three of the six species: tooth ( r = 0.535, 18 d.f.; P<0.05); cerith (r = 0.670, 17
d.f.; P<0.05); and bubble (r = 0.500, 18 d.f.; P<0.05) (Table 8).
DISCUSSION
The results showed that large crabs usually find and inhabit large shells; smaller crabs are
likely to be found in smaller shells. The study was done in a protected area which is closed to
the public and from which shells are not removed; thus hermit crabs in this area appear to be able
to find an adequate range of shell sizes.
114
Leg length was correlated with crab weight in all six species tested; perhaps leg length
could be used as a surrogate of crab size in future studies, precluding the necessity of removing
the crabs from their shells.
The hermit crabs using tooth shells were the fastest and also the strongest among the six
species tested; hermit crabs using cerith shells were the slowest and exerted the weakest pulling
force. The positive correlation between velocity of hermit crabs with and without the shell
indicates that hermit crabs with the greatest speed while carrying their shell were also fastest
without the shell. Thus it is appears not to be the case that tooth shells enable the crabs to move
more swiftly than they would with other shells, but that the swiftest crabs choose tooth shells.
Likewise, crabs that exerted the strongest pulling force did so both while carrying their shell and
after extraction from their shell. Hence the characteristics of tooth shells do not appear facilitate
pulling strength, but rather stronger crabs appear to choose tooth shells.
The weight of shell and the weight of crab were correlated within the tooth shells, but not
within other shell species, which indicates that hermit crabs using tooth shells are usually able to
find a shell proportionate to their weight. As hermit crabs are known to compete with one
another for shells (Bertness 1981), it may be that the fastest and strongest crabs, which appear to
choose tooth shells preferentially, are able to obtain shells that fit well, and to change them as
needed as they grow.
When tested without shells, crab velocity and pulling force showed a positive correlation
in four out of six species, which indicates that, among these species, the fastest individual hermit
crabs are also the strongest. On the other hand, when tested with shells, only three out of six
species showed a correlation between velocity and force.
According to a recent study carried out on shell use by hermit crabs in San Miguel
Biological Station (Estevez-Olea et al. 2012), a total of 33 species of shells were used by hermit
crabs. The two most frequently used shell types were tooth shells, Nerita scabricosta, which
were carried by 45.9% of the hermit crabs sampled, and the rock shell, Acanthais brevidentata,
which accounted for 8.3% of the shells used. The remaining four species tested in our study
were used less commonly: turban shells, Turbo saxosus, made up 3.8% of the crab shells
sampled; ceriths, Cerithium muscarum, 2.8%; bubble shells, Bulla punctulata, 0.4%; and land
snail shells 0.2%.
Tooth shells, which were found to be the preferred shell species in the study of Estevez-
Olea et al. (2012), demonstrated the best performance in terms of crab speed and strength in our
study. Size, however, may be an important determinant of performance: tooth shells had the
greatest mean size in our study, and our results indicate that larger crabs in general were faster
and stronger than small crabs.
Tooth shells, however, were inferior to rock shells, turbans, and ceriths in term of
resistance to crushing. It may be that resistance to crushing is of lesser importance to the crabs
than size, speed, and strength in terms of shell choice.
115
In a study of Coenobita compressus hermit crabs on Isabel Island, Mexico, Osorno et al.
(1998) found that the tooth shell Nerita scabricosta was the preferred shell species, and noted
that these shells had the highest internal volume/weight ratio. Observations of aggressive
interactions between crabs in the field as well as experimental manipulations in which crabs were
induced to change shells confirmed the preference for large shells and for shells with a high
internal volume/weight ratio (Osorno et al. 1998). While tooth shells are the preferred shell
species of hermit crabs in our study area (Estevez-Olea et al. 2012) and were found to be among
the largest shells in our samples, we did not measure the internal volume of the shells and cannot
therefore analyze the ratio of internal volume to weight.
The two shell types which were the thinnest and the least resistant to crushing were land
snails and bubble shells, which, of the six species in our study, were favored least by hermit
crabs (Estevez-Olea et al. 2012). In addition to being more susceptible to breakage, thin shells
provide less protection against dessication (Osorno et al. 2005).
It is noteworthy that the thinness and weakness of terrestrial snail shells reflects the
environment experienced by the gastropods which produce those shells; living on land, they are
not subject to wave action, nor the grinding of pebbles and sand from ocean currents, nor
predation by fish. Bubble shells, which are also comparatively thin and weak, are produced as
vestigial internal shells by a tectobranch sea hare, and as such do not serve to protect the
gastropod in the same way as do the shells of the other marine species.
ACKNOWLEDGEMENTS
We wish to express our deep appreciation to Diana Lieberman of California State
University, Monterey Bay and Milton Lieberman of the Ministry of the Environmental
(MINAET), Costa Rica for their thorough support and assistance throughout the study, both in
the laboratory and in the field. In addition they provided climate data, assisted with data
analysis, and provided editorial support. We thank Dean Philpot, graduate student at Essex
University, for his assistance in acquiring food for the hermit crabs. CSU-LSAMP is supported
by the National Science Foundation under Grant No. HRD-0802628 and the CSU Office of the
Chancellor.
LITERATURE CITED
ANGEL, J.E. 2000. Effects of shell fit on the biology of the hermit crab Pagurus longicarpus
(Say). Journal of Experimental Marine Biology and Ecology 243: 169-184.
APPELTANS, W., BOUCHET, P., BOXSHALL, G.A., DE BROYER, C., DE VOOGD, N.J.,
GORDON, D.F., HOEKSEMA, B.W., HORTON, T., KENNEDY, M., MEES, J., POORE,
G.C.B., READ, G., STÖHR, S., WALTER, T.C., COSTELLO, M.J. (Eds.). 2012. World
Register of Marine Species. Accessed at http://www.marinespecies.org on 2013-04-22.
116
BERTNESS, M. 1981. Competitive dynamics of a tropical hermit crab assemblage. Ecology 62:
751-761.
ESTEVEZ-OLEA, A., RIOS, A., BLAYLOCK, A. & SCHOTTE, P. 2012. Shell utilization by
tropical hermit crabs under strongly contrasting levels of protection and accessibility. Pp. 14-41
in Lieberman, D. & Leiker, S. (eds.), Expedition Report: CSU-LSAMP Costa Rica Research
Program, Summer 2012. California State University Monterey Bay, Seaside, CA.
KEEN, A.M. 1971. Sea Shells of Tropical West America. Second edition. Stanford University
Press, Stanford, CA.
LABARBERA, M. & MERZ, R.A. 1992. Postmortem changes in strength of gastropod shells:
Evolutionary implications for hermit crabs, snails, and their mutual predators. Paleobiology 18:
367-377.
OSORNO, J.L., CONTRERAS-GUARDUÑO, J. & MACIAS-GARCIA, C. 2005. Long-term
costs of using heavy shells in terrestrial hermit crabs (Coenobita compressus) and the limits of
shell preference: an experimental study. Journal of Zoology 266(4):377-383.
OSORNO, J.L., FERNÁNDEZ-CASILLAS, L. & RODRÍGUEZ-JUÁREZ, C. 1998. Are hermit
crabs looking for light and large shells?: evidence from natural and field induced shell
exchanges. Journal of Experimental Marine Biology and Ecology 222(1-2):163-173.
PECHENIK, J. & LEWIS, S. 2000. Avoidance of drilled gastropod shells by the hermit crab
Pagurus longicarpus at Nahant, MA. Journal of Experimental Marine Biology and Ecology
253:17-32.
VANCE, R.R. 1972. The role of shell adequacy in behavioral interactions involving hermit
crabs. Ecology 53: 1075-1083.
117
Table 1. Correlation coefficients and regression formulas for measures of crab size and
performance. Data from all six species are pooled. Weight is measured in grams (g), length in
millimeters (mm), velocity in centimeters per second (cm/s), and force in pound-feet (lbf)
(P<0.05 for all tests shown).
All six species pooled
Tests
d.f. r Regression formulas
Weight of crab vs. weight of shell 236 0.516 Y= 0.864x–0.711
Weight of crab(with shell) vs. leg length 236 0.711 Y = 1.206x+15.937
Weight of crab vs. leg length 236 0.732 Y= 0.164x-1.941
Weight of crab(with shell) vs. velocity (with
shell)
118 0.211 Y= 0.264x+1.686
Weight of crab vs. velocity 99 0.415 Y= 1.180x+4.079
Velocity vs. leg length (with shell) 118 0.528 Y= 0.220x+1.703
Velocity vs. leg length (without shell) 99 0.516 Y= 0.228x+0.882
Force vs. weight of crab (with shell) 118 0.641 Y= 0.030x+0.024
Force vs. weight of crab (without shell) 104 0.525 Y= 0.038x+0.045
Force vs. leg length (without shell) 104 0.621 Y= 0.007x+0.051
Velocity (with shell) vs. velocity (without
shell)
99 0.603 Y= 0.579x+3.165
Force (with shell) vs. force (without shell) 104 0.667 Y= 0.416x+0.024
Velocity vs. force (with shell) 118 0.497 Y= 31.015x+4.196
Velocity vs. force (without shell) 99 0.636 Y= 25.243x+3.167
118
Table 2. Correlation coefficients and regression formulas for shell characteristics and resistance
to crushing for all six shell species pooled. Weight of shell is measured in grams (g), crushing
weight in pounds (lbs), length and width in millimeters (mm) (P<0.05 for all tests shown).
All six species pooled
Tests
d.f. r Regression formulas
Crushing weight vs. weight of shell 235 0.732 Y= 3.247x+15.494
Crushing weight vs. thickness of shell body 117 0.514 Y = 30.568x+12.352
Thickness of aperture vs. thickness of shell body 117 0.510 Y= 0.706x+0.392
Aperture width vs. aperture length 118 0.572 Y= 1.108x + 3.139
Shell width vs. shell length 118 0.698 Y= 0.494x + 0.190
Table 3. Correlation coefficients and regression formulas for crab weight (g) vs. leg length (mm)
for hermit crabs carrying each shell species. Shell species are analyzed individually. There was
a positive correlation for all six species (P<0.05 for all tests).
Within Species
Weight of crab vs. leg length
d.f. r Regression formulas
Cerith 38 0.675 Y= 0.137x-1.038
Tooth 38 0.812 Y= 0.286x-4.333
Turban 37 0.537 Y= 0.366x-4.961
Rock 37 0.591 Y= 0.118x-1.254
Bubble 38 0.519 Y= 0.053x-0.257
Land 37 0.520 Y= 0.099x-0.800
Table 4. Correlation coefficients and regression formulas for analyses of velocity (cm/s) as a
function of crab weight (g)and leg length (mm) (P<0.05 for all tests shown). Shell species are
analyzed individually.
Within Species
Weight of crab vs. velocity (without shell)
d.f. r Regression formulas
Cerith 18 0.781 Y= 3.624x+1.525
Land 18 0.702 Y= 2.781x+1.850
Weight of crab vs. velocity (with shell)
Cerith 18 0.682 Y= 0.967x+2.407
Bubble 18 0.445 Y= 0.888x+4.171
Velocity of crab(without shell) vs. leg length
Cerith 18 0.691 Y= 0.296x-0.044
119
Table 5. Correlation coefficients and regression formulas for analyses of pulling force (lbf) as a
function of crab weight (g) and leg length (mm) (P<0.05 for all tests shown). Shell species are
analyzed individually.
Within Species
Weight of crab vs. force (without shell)
d.f. r Regression formulas
Cerith 18 0.748 Y= 0.066x+0.002
Turban 18 0.543 Y= 0.043x+0.078
Force vs. leg length (without shell)
Cerith 15 0.640 Y= 0.005x-0.025
Weight of crab vs. force (with shell)
Cerith 18 0.904 Y= 0.020x-0.001
Tooth 18 0.634 Y= 0.012x+0.038
Rock 18 0.528 Y= 0.014x+0.024
Bubble 18 0.685 Y= 0.016x+0.010
Land 18 0.598 Y= 0.019x+0.017
Table 6. Weight of crab with shell and the leg length showed a positive correlation in all six
species. Correlation coefficients and regression formulas are listed below for those that
correlated (P<0.05 for all tests). Shell species are analyzed individually.
Within Species
Weight of crab vs. leg length (with shell)
d.f. r Regression formulas
Cerith 38 0.791 Y= 2.824x+9.647
Tooth 38 0.879 Y= 1.673x+16.304
Turban 38 0.740 Y= 0.860x+18.954
Rock 37 0.722 Y= 3.127x+11.856
Bubble 38 0.798 Y= 5.203x+9.363
Land 37 0.631 Y= 2.592x+14.060
120
Table 7. Correlation coefficients and regression formulas for analyses of crab velocity (cm/s) as
a function of crab weight (g) and leg length (mm) (P<0.05 for all tests shown). Shell species are
analyzed individually.
Within Species
Velocity vs. force (without shell)
d.f. r Regression formulas
Cerith 14 0.844 Y= 45.401x+1.935
Tooth 18 0.673 Y= 21.9812x+3.516
Rock 17 0.591 Y= 29.896x+2.456
Velocity vs. force (with shell)
Cerith 18 0.731 Y= 47.142x+2.500
Rock 17 0.561 Y= 53.339x+3.245
Land 18 0.450 Y= 40.394x+3.892
Velocity with shell vs. velocity without shell
Cerith 14 0.808 Y= 0.879x+0.569
Tooth 18 0.567 Y= 0.548x+4.044
Turban 16 0.531 Y= 0.456x+3.703
Rock 17 0.552 Y= 0.730x+2.797
Land 8 0.740 Y= 0.601x+3.554
Force with shell vs. force without shell
Cerith 15 0.893 Y= 0.682x+0.006
Tooth 18 0.557 Y= 0.420x+0.034
Rock 17 0.813 Y= 0.573x+0.015
land 11 0.715 Y= 1.641x+0.002
121
Table 8. Correlation coefficients and regression formulas for shell characteristics and resistance
to crushing for all six shell species. Shell species are analyzed individually. Weight of shell was
measured in grams; crushing weight in lbs; and measurements of length, width, and thickness in
mm (P<0.05 for all tests shown).
Within Species
Aperture thickness vs. thickness of shell
body
d.f. r Regression formulas
Cerith 17 0.659 Y= 0.761x+0.277
Tooth 18 0.633 Y= 0.991x+0.684
Aperture width vs. aperture length
Cerith 18 0.915 Y= 1.335x+0.578
Tooth 18 0.835 Y= 1.409x-1.079
Turban 18 0.934 Y= 1.142x+0.584
Rock 18 0.950 Y= 1.226x+1.718
Bubble 18 0.917 Y= 2.070x+3.892
Land 18 0.910 Y= 1.097x+0.188
Crushing weight vs. thickness of shell body
Cerith 17 0.670 Y= 89.561x+34.997
Tooth 18 0.535 Y= 51.308x+23.043
Bubble 18 0.500 Y= 57.421x+28.333
Shell width vs. shell length
Tooth 18 0.987 Y= 0.654x-0.120
Turban 18 0.930 Y= 0.610x+0.106
Rock 18 0.982 Y= 0.525x+0.002
Bubble 18 0.950 Y= 0.495x+0.112
Land 18 0.767 Y= 0.286x+0.487
122
(a) (b)
(c) (d)
(e) (f)
Figure 1. Individuals were selected to represent a wide range of sizes within each shell species.
(a) Turban shell; (b) Tooth shell (c) Rock shell; (d) Cerith shell; (e) Bubble shell; (f) Land snail
shell.
123
Figure 2a. Force track, viewed from above; a turban shell is attached to the force gauge with
pink string which is held in place on the shell with yellow duct tape. The track measures 5 x 15
x 7 cm.
Figure 2b. Hermit crabs without the shell were harnessed to the force gauge with a string tied
around the abdomen.
Figure 3. The velocity track was located in coastal forest approximately 25 m from shore.
124
Figure 4a. Mean weight of hermit crabs without the shell for crabs carrying each shell species.
Letters below each species indicate which shell types differed statistically in weight; those that
share a letter did not differ from one another. The land snail shells, rock shells, ceriths, and
bubble shells contained the lightest crabs, while the tooth shells and turban shells were carried by
the heaviest crabs.
0
0.5
1
1.5
2
2.5
3
3.5
4
4.5
Land Rock Cerith Bubble Tooth Turban
Mea
n w
eig
ht
of
cra
b (
g)
a a,b a,b b c
c
125
Weight of hermit crab plus shell (g)
Figure 4b. Frequency distributions of weights (g) of hermit crabs using six species of shells.
Data ordered from the lightest crabs (top, wearing land snail shells) to the heaviest crabs
(bottom, wearing tooth shells). Weights include the crab plus the shell.
-1
1
3
5
7
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Land
-1
1
3
5
7
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Rock
0
2
4
6
8
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Cerith
-1
1
3
5
7
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Bubble
-1
1
3
5
7
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Tooth
126
Figure 5a. Mean velocity (cm/s) for hermit crabs using each shell species. Letters below each
species indicate which shell types differed statistically in velocity; those that share a letter did
not differ from one another. Crabs carrying cerith shells showed the lowest velocity while the
crabs carrying the turbans and tooth shells showed the highest velocity.
0.000
1.000
2.000
3.000
4.000
5.000
6.000
7.000
8.000
Cerith Land Rock Bubble Turban Tooth
Mea
n v
elo
city
(cm
/s)
a b b b b,c
c
127
Velocity (cm/sec)
Figure 5b. Frequency distributions of velocity of hermit crabs (cm/sec) carrying each of six
shell species. Species are ranked in order of mean velocity, from the slowest (top, ceriths) to the
fastest (bottom, tooth shells).
0
2
40
0.5 1
1.5 2
2.5 3
3.5 4
4.5 5
5.5 6
6.5 7
7.5 8
8.5 9
9.5
10
10.5 11
11.5 12
12.5 13
13.5 14
14.5 15
Cerith
0
2
4
0
0.5 1
1.5 2
2.5 3
3.5 4
4.5 5
5.5 6
6.5 7
7.5 8
8.5 9
9.5
10
10.5 11
11.5 12
12.5 13
13.5 14
14.5 15
Land
0
2
4
0
0.5 1
1.5 2
2.5 3
3.5 4
4.5 5
5.5 6
6.5 7
7.5 8
8.5 9
9.5
10
10.5 11
11.5 12
12.5 13
13.5 14
14.5 15
Rock
0
2
4
0
0.5 1
1.5 2
2.5 3
3.5 4
4.5 5
5.5 6
6.5 7
7.5 8
8.5 9
9.5
10
10.5 11
11.5 12
12.5 13
13.5 14
14.5 15
Bubble
0
2
4
0
0.5 1
1.5 2
2.5 3
3.5 4
4.5 5
5.5 6
6.5 7
7.5 8
8.5 9
9.5
10
10.5 11
11.5 12
12.5 13
13.5 14
14.5 15
Turban
0
2
4
0
0.5 1
1.5 2
2.5 3
3.5 4
4.5 5
5.5 6
6.5 7
7.5 8
8.5 9
9.5
10
10.
5
11
11.
5
12
12.
5
13
13.
5
14
14.
5
15
Tooth
128
Figure 6a. Mean pulling force (lbf) exerted by hermit crabs bearing shells of each species.
Letters below each species indicate which shell types differed statistically in pulling force; those
that share a letter did not differ from one another. Crabs carrying the cerith, land, rock, and
bubble shells were the weakest while the crabs carrying turbans and tooth shells were the
strongest.
0.000
0.010
0.020
0.030
0.040
0.050
0.060
0.070
0.080
0.090
0.100
Cerith Land Rock Bubble Turban Tooth
Mea
n fo
rce
exer
ted
(lb
f)
a a a a b
b
129
Pulling force (lbf)
Figure 6b. Frequency distributions of pulling force shown by hermit crabs using each of six
shell species. Species are ranked in order of mean pulling strength, from the weakest (top,
ceriths) to the strongest (bottom, tooth shells).
-2
3
80
0.01
0.02
0.03
0.04
0.05
0.06
0.07
0.08
0.09 0.
1
0.11
0.12
0.13
0.14
0.15
0.16
0.17
0.18
0.19 0.
2
0.21
0.22
0.23
0.24
0.25
Cerith
-2
3
8
0
0.01
0.02
0.03
0.04
0.05
0.06
0.07
0.08
0.09 0.
1
0.11
0.12
0.13
0.14
0.15
0.16
0.17
0.18
0.19 0.
2
0.21
0.22
0.23
0.24
0.25
Land
-2
3
8
0
0.01
0.02
0.03
0.04
0.05
0.06
0.07
0.08
0.09 0.
1
0.11
0.12
0.13
0.14
0.15
0.16
0.17
0.18
0.19 0.
2
0.21
0.22
0.23
0.24
0.25
Rock
-2
3
8
0
0.01
0.02
0.03
0.04
0.05
0.06
0.07
0.08
0.09 0.
1
0.11
0.12
0.13
0.14
0.15
0.16
0.17
0.18
0.19 0.
2
0.21
0.22
0.23
0.24
0.25
Bubble
-2
3
8
0
0.01
0.02
0.03
0.04
0.05
0.06
0.07
0.08
0.09 0.
1
0.11
0.12
0.13
0.14
0.15
0.16
0.17
0.18
0.19 0.
2
0.21
0.22
0.23
0.24
0.25
Turban
-2
3
8
0
0.0
1
0.0
2
0.0
3
0.0
4
0.05
0.0
6
0.0
7
0.0
8
0.0
9
0.1
0.1
1
0.1
2
0.1
3
0.1
4
0.15
0.1
6
0.1
7
0.1
8
0.1
9
0.2
0.2
1
0.2
2
0.2
3
0.2
4
0.2
5Tooth
[Escriba una cita del documento o el resumen de un punto interesante. Puede
situar el cuadro de texto en cualquier lugar del documento. Use la ficha
Herramientas de dibujo para cambiar el formato del cuadro de texto de la cita.]
130
Figure 7a. Mean weight necessary for crushing shells of each species. Vertical scales show
weight in lb (left side of graph) and kg (right side of graph). Rock shells and turbans are most
resistant to crushing, while land snail shells and bubble shells are the least resistant.
131
Crushing weight of shell (lb)
Figure 7b. Frequency distributions for each of the six shell species of the weight (lb) necessary
to crush shells. Species are ranked from top (land snails, easiest to crush) to bottom (rock shells,
most resistant to crushing).
0
5
10
15
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100105110115120
Land
0
5
10
15
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100105110115120
Bubble
0
5
10
15
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100105110115120
Tooth
0
5
10
15
0 10 20 30 40 50 60 70 80 90 100 110 120
Cerith
0
5
10
15
0 10 20 30 40 50 60 70 80 90 100 110 120
Turban
0
5
10
15
0 10 20 30 40 50 60 70 80 90 100 110 120
Rock
132
133
Biodiversity
Summary classification of living things observed by participants on the CSU-LSAMP
Costa Rica Research Program, Summer 2012
DOMAIN Archaea
Kingdom Archaebacteria (single cells; cells lack a true nucleus; found in extreme habitats)
(thermophilic bacteria, hot springs bacteria)
DOMAIN Bacteria
Kingdom Eubacteria (cyanobacteria, blue-green algae)
DOMAIN Eukaryota
Kingdom Protista (protozoans; single cells or very simple architecture)
Phylum Foraminifera (forams)
Phylum Dinoflagellata (dinoflagellates)
Phylum Bacillariophyta (diatoms)
Phylum Chlorophyta (green algae)
Phylum Phaeophyta (brown algae)
Phylum Rhodophyta (red algae)
Kingdom Plantae (plants; multicellular; make complex molecules photosynthesis)
Division Bryophyta (mosses)
Division Hepatophyta (liverworts)
Division Pterophyta (ferns)
Division Coniferophyta (conifers)
Division Anthophyta (flowering plants)
Class Monocotyledones (monocots; grasses, palms, orchids, bromeliads, heliconias)
Class Dicotyledones (dicots; black pepper, avocadoes, beans, citrus, coffee, melastomes)
Kingdom Fungi (fungi; multicellular; digest food outside body, then absorb nutrients into tissues)
Division Ascomycota (sac fungi)
Division Basidiomycota (club fungi)
Lichens (symbiotic associations of algae and fungi)
Kingdom Animalia (animals; multicellular; ingest food, break it down inside the body)
Phylum Porifera (sponges)
Phylum Cnidaria
Class Hydrozoa (hydrozoan corals, hydras)
Class Scyphozoa (jellyfish)
Class Anthozoa (sea anemones and corals)
Phylum Turbellaria (free-living flatworms)
Phylum Annelida (segmented worms)
Class Oligochaeta (oligochaetes, earthworms)
Class Polychaeta (polychaetes, marine worms)
134
Phylum Mollusca (mollusks)
Class Polyplacophora (chitons)
Class Gastropoda (snails, slugs)
Class Bivalvia (bivalves)
Class Cephalopoda (octopus)
Phylum Arthropoda (arthropods)
Class Arachnida (spiders, scorpions)
Class Crustacea (lobsters, shrimp, crabs, barnacles, isopods)
Class Diplopoda (millipedes)
Class Chilopoda (centipedes)
Class Insecta (insects)
Phylum Sipunculida (peanut worms)
Phylum Phoronida (phoronids)
Phylum Bryozoa (bryozoans)
Phylum Echinodermata (echinoderms)
Class Asteroidea (sea stars, starfish)
Class Ophiuroidea (brittle stars)
Class Echinoidea (sea urchins)
Class Holothuroidea (sea cucumbers)
Phylum Chordata (chordates)
Subphylum Vertebrata (vertebrates)
Class Chondrichthyes (sharks, rays)
Class Osteichthyes (bony fishes)
Class Amphibia (amphibians, frogs, toads, salamanders)
Class Reptilia (reptiles, turtles, lizards, snakes)
Class Aves (birds)
Class Mammalia (mammals)
Order Marsupialia (opossums)
Order Xenarthra (armadillos, anteaters)
Order Artiodactyla (deer, pigs)
Order Carnivora (raccoons, weasels, dogs, cats)
Order Chiroptera (bats)
Order Rodentia (mice, rats, agoutis, squirrels)
Order Perissodactyla (horses)
Order Primates (monkeys, humans)
135
Gastropod Sightings
Patellogastropoda
Fissurellidae (Keyhole Limpets)
Acmaeidae (Limpets)
Orthogastropoda
Neritamorphia
Neritidae (Tooth Shells)
Vestigastropoda
Trochidae (Top Shells)
Turbinidae (Turban Shells)
Caenogastropoda
Littorinidae (Periwinkles)
Turritellidae (Turret Shells)
Architectonicidae (Sundials)
Vermetidae (Worm Shells)
Planaxidae (Planaxids)
Cerithiidae (Ceriths)
Calyptraeidae (Slipper Shells)
Strombidae (Conchs)
Cypraeidae (Cowries)
Ovulidae (Egg Shells)
Triviidae (Coffee Bean Shells)
Naticidae (Moon Shells)
Cassididae (Helmet Shells)
Cymatiidae (Tritons, Distorsios)
Bursidae (Frog Shells)
Tonnidae (Tun Shells)
Caenogastropoda, [Neogastropoda]
Muricidae (Rock Shells)
Columbellidae (Dove Shells)
Buccinidae (Whelks)
Fasciolariidae (Spindles, Tulips)
Olividae (Olive Shells)
Mitridae (Mitre Shells)
Vasidae (Vase Shells)
Harpidae (Harp Shells)
Conidae (Cone Shells)
Terebridae (Auger Shells)
Heterobranchia
Nudibranchia, Sea Slugs
Pleurobranchia, Sea Hares
Pulmonata, Siphonarias
Nerita scabricosta, San Miguel
Siphonaria gigas, San Miguel
136
Reptile and
Amphibian Sightings
Frogs and toads
Cane toad
Blue jeans poison dart frog
Black and green poison dart frog
Lizards
Wandering gecko
Green basilisk
Green iguana
Black iguana, spiny-tailed iguana or
ctenosaur
Pacific anole
Central American ameiva
Brown spiny lizard
Snakes
Green vine snake
Yellow-bellied sea snake
Eyelash pit viper
Fer-de-lance
Bushmaster
Chunk-headed snake
Road-guard snake
Sea turtles
Olive Ridley sea turtle
Hawksbill turtle
Pacific green turtle
Crocodiles
American crocodile
Caiman
137
Mammal Sightings
Order Didelphimorphia, opossums
Central American Woolly Opossum
Order Xenarthra, sloths and anteaters
Brown-throated Three-toed Sloth
Hoffmann’s Two-toed Sloth
Northern Tamandua or Anteater
Nine-banded Armadillo
Order Artiodactyla, even-toed ungulates
White-tailed Deer
Domestic Pig
Domestic Cattle
Domestic Goat
Order Carnivora, cats, dogs, weasels
Northern Raccoon
White-nosed Coati
Kinkajou
Jaguarundi
Domestic cat, domestic dog
Order Chiroptera, bats
Bats (many species!)
Order Rodentia, rodents
Neotropical Variegated Squirrel
Central American Agouti
Order Perissodactyla, odd-toed ungulates
Domestic Horse
Order Primates, monkeys, humans
White-faced Capuchin Monkey
Mantled Howler Monkey
Northern Tamandua or Anteater
Nine-banded Armadillo
White-nosed Coati
138
Bird Sightings
Pelecanidae, Pelicans
Brown Pelican
Phalacrocoracidae, Cormorants
Neotropic Cormorant
Fregatidae, Frigatebirds
Magnificent Frigatebird
Ardeidae, Herons
Cattle Egret
Bare-throated Tiger-heron
Yellow-crowned Night-heron
Little Blue Heron
Cathartidae, Vultures
Turkey Vulture
Black Vulture
Accipitridae, Hawks
Osprey
White Hawk
American Swallow-tailed Kite
Cracidae, Guans
Great Curassow
Crested Guan
Black Guan
Rallidae, Rails
Gray-necked Wood-rail
Haematopodidae, Oystercatchers
American Oystercatcher
Scolopacidae, Shorebirds
Whimbrel
Columbidae
Rock Dove
Inca Dove
White-winged Dove
White-tipped Dove
Psittacidae, Parrots
Orange-fronted Parakeet
Orange-chinned Parakeet
Red-lored Parrot
Scarlet Macaw
Cuculidae, Cuckoos
Groove-billed Ani
Trochilidae, Hummingbirds
Violet Sabrewing
Rufous-tailed Hummingbird
Purple-throated Mountain-gem
Trogonidae, Trogons
Resplendant Quetzal
Momotidae, Motmots
Blue-crowned Motmot
Turquoise-browed Motmot
Alcedinidae, Kingfishers
Amazon Kingfisher
Ringed Kingfisher
Ramphastidae, Toucans
Keel-billed Toucan
Picidae, Woodpeckers
Pale-billed Woodpecker
139
Formicariidae, Antbirds
Barred Antshrike
Tyrannidae, Flycatchers
Tropical Kingbird
Social Flycatcher
Great Kiskadee
Dusky-capped Flycatcher
Corvidae, Jays
Brown Jay
White-throated Magpie-jay
Azure-hooded Jay
Troglodytidae, Wrens
Rufous-and-white Wren
Plain Wren
Southern House Wren
Sylviidae, Gnatcatchers
Tropical Gnatcatcher
Turdidae, Thrushes
Clay-colored Thrush
Slaty-backed Nightingale-thrush
Mountain Robin
Black-faced Solitaire
Thraupidae, Tanagers
Blue-gray Tanager
Spangled-cheeked Tanager
Scarlet-rumped Tanager
Icteridae, Orioles
Great-tailed Grackle
Montezuma Oropendola
Baltimore Oriole
Emberizidae, Sparrows
Variable Seedeater
Blue and White Swallow
Mangrove Swallow
Rufous-collared Sparrow
Yellow-crowned Night-herons, San Miguel
140
Fish Sightings Urolophidae
Round Stingray
Muraenidae, Moray Eels
Jeweled Moray
Palenose Moray
Gobiesocidae, Clingfishes
Elegant Clingfish
Holocentridae, Squirrelfishes
Tinsel Squirrelfish
Scorpaenidae, Scorpionfishes
Spotted Scorpionfish
Serranidae, Groupers
Flag Cabrilla
Panama Graysby
Banded Serrano
Apogonidae, Cardinalfishes
Plain Cardinalfish
Tailspot Cardinalfish
Carangidae, Jacks
Blue Crevalle
Pacific Crevalle
Lutjanidae, Snappers
Barred Pargo
Yellow Snapper
Dog Snapper
Colorado Snapper
Spotted Rose Snapper
Gerridae, Mojarras
Yellowfin Mojarra
Blackspot Mojarra
Kyphosidae, Chubs
Cortez Chub
Haemulidae, Grunts
Silvergrey Grunt
Burrito Grunt
Mojarra Grunt
Greybar Grunt
Spottail Grunt
Chaetodontidae, Butterflyfishes
Threebanded Butterflyfish
Barberfish
Pomacanthidae, Angelfishes
Cortez Angelfish
Cirrhitidae, Hawkfishes
Giant Hawkfish
Muglidae, Mullets
Thick-Lipped Mullet
White Mullet
Pomacentridae, Damselfishes
Panamic Nightsergeant
Panamanian Sergeant Major
Giant Damselfish
Acapulco Gregory
Beaubrummel Gregory
141
Labridae, Wrasses
Mexican Hogfish
Chameleon Wrasse
Spinster Wrasse
Banded Wrasse
Cortez Rainbow Wrasse
Scaridae, Parrotfishes
Azure Parrotfish
Labrisomidae, Weed Blennies
Margarita Blenny
Chaenopsidae, Tube Blennies
Hancocks Tube Blenny
Blennidae, Blennies
Panamic Fanged Blenny
Sabertooth Blenny
Acanthuridae, Surgeonfishes
Yellowfin Surgeonfish
Chancho Surgeofish
Balistidae, Triggerfishes
Blunthead Triggerfish
Tetraodontidae, Pufferfishes
Spotted Green Puffer
Blue-Phase Guineafowl Puffer
Golden Phase Guineafowl Puffer
Spotted Sharpnose Puffer
Diodontidae, Porcupinefishes
Porcupinefish
Spotted Sharpnose Puffer, San Miguel
142
Personal “Firsts” ≈ new experiences
Traveling outside the U.S. / having a passport / being over 150 miles from home
being away from home for more than 2 weeks
swimming in the Pacific ocean / in a hot spring / under a waterfall
jumping into a river from a rope swing
hiking along a volcano / in a tropical forest / in the rain
going on a 5-hour wilderness hike / ziplining through a cloud forest
surfing / body surfing / snorkeling at sunset
climbing a mountain / seeing a crater lake / tubing in a river
being in a country that that speaks another language
using a foreign currency (colones) / rolling my R’s / living with a host family
learning the culture and customs of Costa Rica / milking a cow
having a whole conversation in a foreign language / dancing with a Costa Rican at a disco
eating snails (burgados con arroz) / gallo pinto / platanos con queso
eating real chicharrones / TRITS ice cream / rice and beans on a daily basis
eating guanabana, mamon chino, ensalada de remolacha, and fried yuca
catching my own dinner / cooking tacos for 20+ people / making empanadas
riding in the bed of a truck in the rain (it’s more fun in the rain!)
sleeping next to the ocean / sleeping in the jungle / sleeping in a hammock
waking up to a thunderstorm / duct taping my sandals back together / taking cold showers
playing Frisbee and liking it! / playing volleyball on the beach / playing a mejenga on rocks
seeing howler monkeys, white faced capuchins, crocodiles in the wild
observing reef fishes, Jesus Christ lizard, scarlet macaws, morpho butterflies, a scorpion
seeing a sloth sloooowly eat
letting a golden orb weaver spider walk on me / touching a giant millipede
swimming with a sea turtle / holding a mullet / petting a crawdad
holding a puffer fish / toad / sea cucumber / brittle star / nudibranch
catching fish with my bare hands / being slapped in the face by a tilapia
being a field biologist / mapping a forest / being in an absolute reserve
learning and enjoying statistics / designing and executing a research project
getting up in the middle of the night to catch fish / collecting over 2,000 hermit crabs
participating in a research symposium
143
Cultural Immersion &
Homestay Experiences
Host families:
Marcos Marín / Lorena Leitón (Joseph Barrett)
Yenny Cruz (Nate Bell)
Rafa Leitón / Liliam Arce (Adrienne Blaylock)
Alvaro Vega / Elisa Mata (Juan Carlos de la Parra)
Hugo Picado / Lila Mora (Emilia Escobar)
Olivier Garro / Marielos Cruz (Antonia Estevez)
Miguel Fuentes / Marina Zamora (Dwayne Franco)
Ofelia Rodriguez (Adrianna Hernandez)
Misael Alvarado / Aidee Méndez (Mark Jackson)
Tino Pérez / Anabelli Picado (Danielle Kuperus)
Macho Leitón / Tema Salazar (Amie Nowacki)
William Leitón / Damaris Salazar (Kara Nygaard)
Carlos Fuentes / Flory Bogantes (Jennifer Retana)
Miriam Salazar / Ronald Cruz (Alex Rios)
Geovanny Leitón / Cristina Obando (Katie Sowul)
Koki Fuentes / Lita Rodriguez (Areli Tejeda)
Virginia Leiton (Sheldon Leiker)
Zaida Villalobos (Dean Philpot)
Milton Brenes / Edith Salazar (Phil Schotte)
Observations and analyses by participants:
“I have learned to appreciate each individual of San Luis because they all have unique
stories”.
“Miriam, my host mom, invited me into her home as if I was her own grandchild or son. I
am really appreciative to have had this opportunity”.
“Spending time with the children was definitely my favorite part. We played a lot of
games and the kids cheated on many of them”.
“This morning after breakfast, Misael walked with us to the sugar-mill. The walk was
absolutely beautiful. The path was lined with touch-sensitive plants. It was clear and sunny,
so we could see the mountains all around us, and we walked through fields and woods. It was
amazing”.
144
“This felt like I was at home and not a guest. My host family even teased me, which was
cool!”
“We all have breakfast here together, wake up early, feed the chickens, and get the eggs
that have been laid. If chicken is going to be eaten, then one is killed. Everyone visits each
other throughout the day”.
“My host family has showed me how a real community operates”.
“Even though the children are older they are not ashamed to hug their mother. I like the
fact that there are ‘good people’ like them in the world”.
“The most enjoyable moments I have had with my host mom would be the late nights when
we drank coffee and just talked”.
“My Spanish has gotten better, so I learned that sometimes you just have to talk and it
will work out fine”. You don’t really have to say everything in words. Actions are very
important”.
“Miguelito is pretty much my new BFF. We played for hours yesterday; he’s a real
jokester!!!”
“The past three nights have been extremely fantastic with my host family. I have caught
spiders, seen bats, eaten great food, and learned new words in Spanish”.
“One of the great pleasures I have had here is to work on a coffee plantation, seeing firsthand
how rich both the culture and soil of Costa Rica is. In 80+° weather I sweat like I have never
done before and this kind of work was just a typical chore for Costa Ricans”.
“In San Luis I walk everywhere and say hello to everyone I see. In the United States I
drive everywhere and only say hello to those I know”.
“My host family received many visits by neighbors and family throughout the few days
I was with them--more visits than I receive at home in a month”.
”I have got a glimpse of what it is like to live with very little, but I don’t see that as a bad
thing”.
“In my home town the sounds of the environment are just noise from cars, airplanes, or
helicopters. In San Luis there is always a bird song or insects calling”.
“Food is homemade and it takes time to make, but it tastes so much better and is so much
healthier”.
“Life is timeless here, an oasis where smog and anger don’t exist. No one has an ‘i’ –
anything. What a life!”
“This day encompasses everything that I wanted to do so much: talk with local people
who were my age, play some football, have a delicious dinner, help people of the
community, and go home knowing that my host family would be waiting for me, ready to
ask me how my day was”.
145
“Tonight is the last time I will be sleeping on this bed and tonight is also when I completely
felt part of this family. I took a cold shower without screaming; I finished my plate, went for
seconds, and finished it too; I had hour long conversations with my family after dinner; and
even went to help William put soil in bags for planting coffee”.
“It was very difficult to say goodbye to my host family. My host mom made me
scrambled eggs and added a little cream cheese to my toast. As I ate, she showed me pictures
and gave me a few that were in the album, and we shared a few more stories about our
pasts”.
“My homestay experience has shown me that people can be happy without material
items, even things I have seen as necessities, as long as they stay together and love each
other”.
146
Photographs
147
148
149
150
151
152
153
154
155
156
157
158
159
CSU-LSAMP Costa Rica Summer Research Program, Summer 2012
Front row, left to right: Dean Philpot, Danielle Kuperus, Areli Tejeda, Jennifer Retana, Mark Jackson,
Carlos de la Parra, Phil Schotte. Back row: Alex Rios, Sheldon Leiker, Emily Escobar,
Dwayne Franco, Antonia Estevez, Adrianna Hernandez, Diana Lieberman, Amie Nowacki,
Katie Sowul, Nate Bell, Adrianna Blaylock, Kara Nygaard, Jacob Barrett.
