Annals of Aquaculture and Research

The Reported Occurrence of Hermaphroditism in the Yellowfoot Limpet (Cellana sandwicensis Pease, 1981)

Short Communication | Open Access

  • 1. Department of Molecular Biosciences and Bioengineering, College of Tropical Agriculture and Human Resources” (CTAHR), University of Hawaii at Manoa, USA
+ Show More - Show Less
Corresponding Authors
Jon-Paul Bingham, Department of Molecular Biosciences and Bioengineering, College of Tropical Agriculture and Human Resources” (CTAHR), University of Hawaii at Manoa, 1955 East West Rd. Agricultural Sciences Rm 218, Honolulu, Hawaii, 96822, USA, Tel: 1-808-956-8384; Fax: 808-956-3542

The yellowfoot limpet Cellana sandwicensis, ‘opihi ‘alinalina, is a significant cultural resource and seafood for Hawaiians. With wild stocks greatly depleted and under significant commercial pressures, research efforts are focused on understanding their reproductive biology to improve management and ensure survival of this species.

During spawning season, wild aquaculture-housed limpets were examined on a monthly basis for sexual maturation, via gonadosomatic index and histological examination. Spawn events, which coincided with peak maturation, were observed. Furthermore, a single specimen was observed to be a hermaphrodite. While hermaphroditism has been a documented reproduction strategy for other Palletid spp., it has never been documented in any of the Hawaiian limpets (Cellana spp.).

Previously, Cellana sandwicensis was assumed to be gonochoristic with males and females. And despite sex ratios shifting across time and geographic location, no clear biological explanation existed for this phenomenon.

From this finding, we propose that the yellowfoot limpet may be a sequential hermaphrodite, which has, until now, gone undetected. This hermaphrodite, although carrying both gonads simultaneously, was most likely caught at an inter-sex level. It is then plausible to consider environmental factors (i.e. presence of conspecifics) playing a role in sex determination for this species.

In the future, defining sex ratios at various class sizes, time points, and geographic locations will improve our understanding of reproductive biology for yellow foot limpets. Moreover, monitoring individuals across multiple spawning events/seasons will clarify any speculation regarding their ability/inability to switch sexes.


Mau A, Fox K, Bingham JP (2017) The Reported Occurrence of Hermaphroditism in the Yellowfoot Limpet (Cellana sandwicensis Pease, 1981). Ann Aquac Res 4(4): 1045.


•    Hermaphroditism
•    Invertebrate
•    Mollusk
•    Sexual reproduction


Nearly all forms of sexual reproduction have been documented for mollusks. In terms of hermaphroditism, some mollusks exhibit simultaneous hermaphroditism, sequential hermaphroditism, or alternating hermaphroditism reproductive strategies [1]. In other cases, the ovo-testis, a small hermaphroditic duct containing both male and female gonad characteristics, is common [2]. Despite this plastic reproductive molluscan nature, only 3% of known species of Eogastropods (formerly Prostobranchs) [3] are functional hermaphrodites [4]. Moreover, hermaphroditism occurs in less than 0.29% of all Patellid species, which is considerably rare [5]. For Patella ferruginea, a well-documented limpet, the minimum size at which sex change occurs is 40-60 mm shell length, and in the male to female direction. For protandrous species like this, size selecting (during harvesting) may negatively impact reproductive output and threaten species survival [6]. Additionally, selecting larger individuals has been reported to cause mediated sex change in smaller sized individuals, which shifts population dynamics [7]. These aspects of hermaphroditism are considerably important for conservation and management efforts for at-risk Patellid species.

The yellowfoot limpet, Cellana sandwicensis, ‘opihi ‘alinalina an at-risk Patellid species, may also exhibit a form of hermaphroditism. Previous research reports that mature limpets maintain separate sexes, gonochoristic. The typical spawning season coincides with the peak of winter, however, occasional spawning events have been recorded during other times of the year [8]. The peak of this spawning season is thought to shift year-to-year depending on the hydrodynamic environment (i.e. temperature, tide, and waves). The sex ratio shifts from being dominated by an unidentifiable sex during resting periods to a near 1:1 male to female ratio in spawning periods [8,9]. However, this interesting phenomenon still lacks a biological explanation. Hence forth, authors aim to show evidence of a bi-directional form of sequential hermaphroditism, and to explain how hermaphroditism may be a significant reproduction strategy for the survival of this Hawaiian limpet.


Yellowfoot limpets (Cellana sandwicensis) were collected from Rabbit Island, Oahu, Hawaii (21°19′52″N 157°39′32″W) to monitor sexual reproduction. Animals (n=45) were stocked at random into a circular flow-through aquaculture system (total tank surface area of 0.6 m2 ) and reared at ambient conditions.

Air temperature (18.51-33.57°C) was recorded in 4 second intervals using HOBO MX1101 Temperature/Relative Humidity Data Logger (Accuracy ± 0.2°C, Onset Computers, Bourne, MA). Seawater temperature (24.65-26.93°C) and dissolved oxygen was measured twice daily and averaged using an YSI Pro20 Dissolved Oxygen Meter (Accuracy ± 0.3°C and ± 0.2 mg L-1, YSI Inc., Yellow Springs, OH). Seawater pH (8.24) was measured once daily using an EcoSense pH10A instrument (YSI Inc., Yellow Springs, OH), and salinity (30 g L-1) was measured once daily using a Vital Sine Refractometer (Accuracy ±1.0%, Pentair, Apopka, FL).

Animals were offered a formulated diet (ad libitum) with access to feed between 16:00 and 08:00 hours. Animals (n=3) were sacrificed monthly to determine maturation status, and at the end of the trial. The reported hermaphrodite specimen was sacrificed at the end of the trial (May), and dissection of this individual revealed the presence of both ovary and testis.

Measurements for shell length and shell width (mm) were done using an electronic caliper (0.01 mm), and measurements for total weight (g), soft-body weight (g), and gonad weight (g) used an electronic scale (0.0001 g, AG104 Mettler-Toledo International, Columbus, OH). The gonadosomatic index (including both ovary and testis) was calculated as follows: GSI = [total gonad weight / total soft body weight] x 100.

Gonad tissue was fixed in 10% v/vneutral buffered formalin for 24 hours at room temperature and rinsed with 70% v/v ethanol. Samples were wax embedded, and 6 µm horizontal sections across the entire length of the gonad were stained with haematoxylin and eosin. Images were captured with Infinity Analyze V 6.5.4 Lumenera Software and Infinity3S-1UR microscopy camera (Lumenera Corporation, Ottawa, ON), and compound microscope Olympus BX43 (Olympus, Center Valley, PA).


The sex ratio during the current spawning season was 1:3 male to female—an egg-rich population. The sex ratio during this study differs from previous literature, which has previously been reported to be 1:1 male to female in two separate studies [8,9]. This may be due to different determinants of sex: environment (i.e. conspecific interaction, temperature and pollution/ pollutants) and/or genetics found across different time scales and geographic locations.

Recently, we surveyed yellowfoot limpets in the Papahanaumokuakea Marine National Monument (a marine reserve in the Northwestern Hawaiian Islands), which appeared to be another egg-rich population (unpublished data); and we postulate that the presence of larger individuals and/or high density aggregates may be factoring in to this phenomenon. More specifically, the sperm to egg ratio may play a role in controlling proper fertilization [10], and therefore influence sex ratios.

During this study, only 1 of 45 samples was found to be hermaphroditic. The specimen’s shell (Figure 1A/2B) was 62.08 mm long and 49.54 mm wide, it is considered a relatively large individual (the average shell length and shell width for this collected group was 37.96 ± 3.76 mm and 29.91 ± 3.24 mm, respectively). The specimen’s total weight was 35.54 g and soft body tissue weight was 10.75 g. The total gonad weight, including both ovary and testis, was 0.68 g; and the GSI was 6.33% at the time of dissection. In March 2017, this individual was observed spawning in the tank environment, naturally. We determined this specimen to be a functioning male based on the release of white colored gametes. However, the presence of female reproductive organs found during dissection provided evidence that this specimen should be classified as a hermaphrodite.

The small sample size and low rate of hermaphroditism (2.22%) may simply be a result of random, genetic mutation acting on this single specimen. However, we must also consider hermaphroditism as a viable reproduction strategy for this species. When considering the classification of hermaphrodites, yellowfoot limpets might be recognized as simultaneous hermaphrodites since both ovary and testis were observed in this specimen. However, histology indicates that this specimen was not a functioning simultaneous hermaphroditism. The testis of this specimen contained mature spermatozoa with gaps in the gonadal cavity indicating a mature/post-spawn stage of gonad development (Figure 3A/3B). The ovary contained primordial germ cell proliferation, indicating an early stage of gonad development for future spawning events (Figure 2A/2B). Because this individual had an immature ovary and functioned as a male during spawning season, it would not be physiologically capable of selfing (self-fertilization) or cross-fertilizing with a mate—a recognizable characteristic of simultaneous hermaphrodites [4].

The apparent sex switch occurring in this individual specimen is most likely a form of sequential hermaphroditism. However, based on current data for yellowfoot limpets, there is no evident bias in sex ratio at any given size class that would indicate this to be a protandrous or protogynous species (unidirectional sex change) [11]. A more feasible theory is that this species maintains a bi-directional form of sequential hermaphroditism—a reproductive strategy found in fish [12], oysters [13], and limpets [14]—that allows switching of sexes in either direction based on environmental influences.

During sex change of sequential hermaphrodites, it is theorized that gonad development is arrested and the animal is not reproductively viable [5]. We explain that the discovery of a specimen carrying both male and female gonads may illustrate a rarely observed intermediate stage during the transition between sexes—where an individual would usually transition into an unidentifiable sex (reduced gonad cavity). We also consider that this specimen appears to sex-switch in a single spawning season, and may have continued developing into a functioning female without a resting phase between the transitions. This would mean that yellowfoot limpets can potentially sex-switch at any given time of the year. However, it appears that the “normal” period where we could expect the sex switching to occur would be between spawning seasons (resting period/offseason).

Interestingly enough, hermaphrodites that switch sex back and forth are only found in broadcast spawning species of marine snails [1]. From an evolutionary perspective, the ability to switch sexes is crucial for the survival of the species when lacking copulatory organs. For yellowfoot limpet, an at-risk species, individuals capable of switching sex based on their available partners allows them to reproduce under adverse conditions (i.e. low densities). We therefore suggest these limpets most likely undergo environmental sex determination—where individuals can influence the sexual status of another conspecific via pheromones— as opposed to genetic sex determination associated with other sequential hermaphrodites [4].

To test this speculative theory, researchers would need to monitor broodstock across multiple spawning seasons to determine if functional sex-switching occurs. And based on the low rate of hermaphroditism, a relatively large number of individuals would be required. Based on our postulated theory, altering the size class and/or densities in the tank environment over time may increase the rate of hermaphroditism. Additionally, frequently sampling throughout the year would potentially increase detectability of direct sex-change (intermediate stage) within a single spawning season.


The yellowfoot limpet (Cellana sandwicensis), is an important traditional cultural and food resource, and a candidate aquaculture species. As part of proper management, conservation, and production, it is imperative to understand the life cycle and mode of reproduction for these marine snails. In this current study, we report a paradigm-shifting discovery, a hermaphrodite individual carrying an ovary and testis. Previous to this study, it has been reported that individuals are of separate sexes, male or female, but hermaphroditism was never observed. Although there were reports of annual shifts in sex ratios, this phenomenon could not be explained. We propose a theory that the yellowfoot limpet is a sequential hermaphrodite and is capable of switching sex in a bi-directional manner dependent on environmental cues.


1. Collin R. Phylogenetic patterns and phenotypic plasticity of molluscan sexual systems. Integr Comp Bio. 2013; 53: 723-735.

2. Lee CH, Kaang BK, Lee YD. Structure and Function of the Reproductive System of Aplysiakurodai. Dev Reprod. 2015; 19: 197–207.

3. Ponder WF, Lindberg DR. Towards a phylogeny of gastropod molluscs: an analysis using morphological characters. Zool J Linnean Soc.1997; 119: 83–265.

4. Heller J. Hermaphroditism in molluscs. Biol J Linnean Soc. 1993; 48: 19-42.

5. Dodd JM. Studies on the biology of limpets: III. Hermaphroditism in the three British species of Patella. J Mar Biol Assoc UK. 1956; 2: 327- 340.

6. Espinosa F, Guerra-Garcia JM, Fa D, Garcia-Gomez JC. Aspects of reproduction and their implications for the conservation of the endangered limpet, Patella ferruginea. Invert Reprod Dev. 2006; 49: 85-92.

7. Rivera-Ingraham GA, Espinosa F, García-Gómez JC. Environmentally mediated sex change in the endangered limpet Patella ferruginea (Gastropoda: Patellidae). J Moll Stud. 2011; 77: 226-231.

8. Kay EA, Corpuz GC, Magruder WH. Opihi. Their biology and culture. Aquaculture. 1982; 180-213.

9. Hua NT, Ako H. Reproductive Biology and Effect of Arachidonic Acid Level in Broodstock Diet on Final Maturation of the Hawaiian Limpet Cellana sandwicensis. Aqua Res Dev. 2014; 5: 1.

10. Levitan DR. The relationship between egg size and fertilization success in broadcast-spawning marine invertebrates. Integr Comp Biol. 2006; 46: 298-311.

11. Allsop DJ, West SA. Sex-ratio evolution in sex changing animals. Evolution. 2004; 58: 1019-1027.

12. Munday PL, Caley MJ, Jones GP, Bi-directional Lee CH, Kaang BK, Lee YD. Structure and Function of the Reproductive System of Aplysia kurodai. Dev Reprod. 2015; 19: 197–207.

13. Yasuoka N, Yusa Y. Direct evidence of bi-directional sex change in natural populations of the oysters Saccostrea kegaki and S. mordax. Plank. 2017; 12: 78-81.

14. Guallart J, Calvo M, Acevedo I, Templado J. Two-way sex change in the endangered limpet Patella ferruginea (Mollusca, Gastropoda). Invert Reprod Dev. 2013; 57: 247-253.

Received : 15 Sep 2017
Accepted : 05 Sep 2017
Published : 07 Oct 2017
Annals of Otolaryngology and Rhinology
ISSN : 2379-948X
Launched : 2014
JSM Schizophrenia
Launched : 2016
Journal of Nausea
Launched : 2020
JSM Internal Medicine
Launched : 2016
JSM Hepatitis
Launched : 2016
JSM Oro Facial Surgeries
ISSN : 2578-3211
Launched : 2016
Journal of Human Nutrition and Food Science
ISSN : 2333-6706
Launched : 2013
JSM Regenerative Medicine and Bioengineering
ISSN : 2379-0490
Launched : 2013
JSM Spine
ISSN : 2578-3181
Launched : 2016
Archives of Palliative Care
ISSN : 2573-1165
Launched : 2016
JSM Nutritional Disorders
ISSN : 2578-3203
Launched : 2017
Annals of Neurodegenerative Disorders
ISSN : 2476-2032
Launched : 2016
Journal of Fever
ISSN : 2641-7782
Launched : 2017
JSM Bone Marrow Research
ISSN : 2578-3351
Launched : 2016
JSM Mathematics and Statistics
ISSN : 2578-3173
Launched : 2014
Journal of Autoimmunity and Research
ISSN : 2573-1173
Launched : 2014
JSM Arthritis
ISSN : 2475-9155
Launched : 2016
JSM Head and Neck Cancer-Cases and Reviews
ISSN : 2573-1610
Launched : 2016
JSM General Surgery Cases and Images
ISSN : 2573-1564
Launched : 2016
JSM Anatomy and Physiology
ISSN : 2573-1262
Launched : 2016
JSM Dental Surgery
ISSN : 2573-1548
Launched : 2016
Annals of Emergency Surgery
ISSN : 2573-1017
Launched : 2016
Annals of Mens Health and Wellness
ISSN : 2641-7707
Launched : 2017
Journal of Preventive Medicine and Health Care
ISSN : 2576-0084
Launched : 2018
Journal of Chronic Diseases and Management
ISSN : 2573-1300
Launched : 2016
Annals of Vaccines and Immunization
ISSN : 2378-9379
Launched : 2014
JSM Heart Surgery Cases and Images
ISSN : 2578-3157
Launched : 2016
Annals of Reproductive Medicine and Treatment
ISSN : 2573-1092
Launched : 2016
JSM Brain Science
ISSN : 2573-1289
Launched : 2016
JSM Biomarkers
ISSN : 2578-3815
Launched : 2014
JSM Biology
ISSN : 2475-9392
Launched : 2016
Archives of Stem Cell and Research
ISSN : 2578-3580
Launched : 2014
Annals of Clinical and Medical Microbiology
ISSN : 2578-3629
Launched : 2014
JSM Pediatric Surgery
ISSN : 2578-3149
Launched : 2017
Journal of Memory Disorder and Rehabilitation
ISSN : 2578-319X
Launched : 2016
JSM Tropical Medicine and Research
ISSN : 2578-3165
Launched : 2016
JSM Head and Face Medicine
ISSN : 2578-3793
Launched : 2016
JSM Cardiothoracic Surgery
ISSN : 2573-1297
Launched : 2016
JSM Bone and Joint Diseases
ISSN : 2578-3351
Launched : 2017
JSM Bioavailability and Bioequivalence
ISSN : 2641-7812
Launched : 2017
JSM Atherosclerosis
ISSN : 2573-1270
Launched : 2016
Journal of Genitourinary Disorders
ISSN : 2641-7790
Launched : 2017
Journal of Fractures and Sprains
ISSN : 2578-3831
Launched : 2016
Journal of Autism and Epilepsy
ISSN : 2641-7774
Launched : 2016
Annals of Marine Biology and Research
ISSN : 2573-105X
Launched : 2014
JSM Health Education & Primary Health Care
ISSN : 2578-3777
Launched : 2016
JSM Communication Disorders
ISSN : 2578-3807
Launched : 2016
Annals of Musculoskeletal Disorders
ISSN : 2578-3599
Launched : 2016
Annals of Virology and Research
ISSN : 2573-1122
Launched : 2014
JSM Renal Medicine
ISSN : 2573-1637
Launched : 2016
Journal of Muscle Health
ISSN : 2578-3823
Launched : 2016
JSM Genetics and Genomics
ISSN : 2334-1823
Launched : 2013
JSM Anxiety and Depression
ISSN : 2475-9139
Launched : 2016
Clinical Journal of Heart Diseases
ISSN : 2641-7766
Launched : 2016
Annals of Medicinal Chemistry and Research
ISSN : 2378-9336
Launched : 2014
JSM Pain and Management
ISSN : 2578-3378
Launched : 2016
JSM Women's Health
ISSN : 2578-3696
Launched : 2016
Clinical Research in HIV or AIDS
ISSN : 2374-0094
Launched : 2013
Journal of Endocrinology, Diabetes and Obesity
ISSN : 2333-6692
Launched : 2013
Journal of Substance Abuse and Alcoholism
ISSN : 2373-9363
Launched : 2013
JSM Neurosurgery and Spine
ISSN : 2373-9479
Launched : 2013
Journal of Liver and Clinical Research
ISSN : 2379-0830
Launched : 2014
Journal of Drug Design and Research
ISSN : 2379-089X
Launched : 2014
JSM Clinical Oncology and Research
ISSN : 2373-938X
Launched : 2013
JSM Bioinformatics, Genomics and Proteomics
ISSN : 2576-1102
Launched : 2014
JSM Chemistry
ISSN : 2334-1831
Launched : 2013
Journal of Trauma and Care
ISSN : 2573-1246
Launched : 2014
JSM Surgical Oncology and Research
ISSN : 2578-3688
Launched : 2016
Annals of Food Processing and Preservation
ISSN : 2573-1033
Launched : 2016
Journal of Radiology and Radiation Therapy
ISSN : 2333-7095
Launched : 2013
JSM Physical Medicine and Rehabilitation
ISSN : 2578-3572
Launched : 2016
Annals of Clinical Pathology
ISSN : 2373-9282
Launched : 2013
Annals of Cardiovascular Diseases
ISSN : 2641-7731
Launched : 2016
Journal of Behavior
ISSN : 2576-0076
Launched : 2016
Annals of Clinical and Experimental Metabolism
ISSN : 2572-2492
Launched : 2016
Clinical Research in Infectious Diseases
ISSN : 2379-0636
Launched : 2013
JSM Microbiology
ISSN : 2333-6455
Launched : 2013
Journal of Urology and Research
ISSN : 2379-951X
Launched : 2014
Journal of Family Medicine and Community Health
ISSN : 2379-0547
Launched : 2013
Annals of Pregnancy and Care
ISSN : 2578-336X
Launched : 2017
JSM Cell and Developmental Biology
ISSN : 2379-061X
Launched : 2013
Clinical Research in Pulmonology
ISSN : 2333-6625
Launched : 2013
Journal of Immunology and Clinical Research
ISSN : 2333-6714
Launched : 2013
Annals of Forensic Research and Analysis
ISSN : 2378-9476
Launched : 2014
JSM Biochemistry and Molecular Biology
ISSN : 2333-7109
Launched : 2013
Annals of Breast Cancer Research
ISSN : 2641-7685
Launched : 2016
Annals of Gerontology and Geriatric Research
ISSN : 2378-9409
Launched : 2014
Journal of Sleep Medicine and Disorders
ISSN : 2379-0822
Launched : 2014
JSM Burns and Trauma
ISSN : 2475-9406
Launched : 2016
Chemical Engineering and Process Techniques
ISSN : 2333-6633
Launched : 2013
Annals of Clinical Cytology and Pathology
ISSN : 2475-9430
Launched : 2014
JSM Allergy and Asthma
ISSN : 2573-1254
Launched : 2016
Journal of Neurological Disorders and Stroke
ISSN : 2334-2307
Launched : 2013
Annals of Sports Medicine and Research
ISSN : 2379-0571
Launched : 2014
JSM Sexual Medicine
ISSN : 2578-3718
Launched : 2016
Annals of Vascular Medicine and Research
ISSN : 2378-9344
Launched : 2014
JSM Biotechnology and Biomedical Engineering
ISSN : 2333-7117
Launched : 2013
Journal of Hematology and Transfusion
ISSN : 2333-6684
Launched : 2013
JSM Environmental Science and Ecology
ISSN : 2333-7141
Launched : 2013
Journal of Cardiology and Clinical Research
ISSN : 2333-6676
Launched : 2013
JSM Nanotechnology and Nanomedicine
ISSN : 2334-1815
Launched : 2013
Journal of Ear, Nose and Throat Disorders
ISSN : 2475-9473
Launched : 2016
JSM Ophthalmology
ISSN : 2333-6447
Launched : 2013
Journal of Pharmacology and Clinical Toxicology
ISSN : 2333-7079
Launched : 2013
Annals of Psychiatry and Mental Health
ISSN : 2374-0124
Launched : 2013
Medical Journal of Obstetrics and Gynecology
ISSN : 2333-6439
Launched : 2013
Annals of Pediatrics and Child Health
ISSN : 2373-9312
Launched : 2013
JSM Clinical Pharmaceutics
ISSN : 2379-9498
Launched : 2014
JSM Foot and Ankle
ISSN : 2475-9112
Launched : 2016
JSM Alzheimer's Disease and Related Dementia
ISSN : 2378-9565
Launched : 2014
Journal of Addiction Medicine and Therapy
ISSN : 2333-665X
Launched : 2013
Journal of Veterinary Medicine and Research
ISSN : 2378-931X
Launched : 2013
Annals of Public Health and Research
ISSN : 2378-9328
Launched : 2014
Annals of Orthopedics and Rheumatology
ISSN : 2373-9290
Launched : 2013
Journal of Clinical Nephrology and Research
ISSN : 2379-0652
Launched : 2014
Annals of Community Medicine and Practice
ISSN : 2475-9465
Launched : 2014
Annals of Biometrics and Biostatistics
ISSN : 2374-0116
Launched : 2013
JSM Clinical Case Reports
ISSN : 2373-9819
Launched : 2013
Journal of Cancer Biology and Research
ISSN : 2373-9436
Launched : 2013
Journal of Surgery and Transplantation Science
ISSN : 2379-0911
Launched : 2013
Journal of Dermatology and Clinical Research
ISSN : 2373-9371
Launched : 2013
JSM Gastroenterology and Hepatology
ISSN : 2373-9487
Launched : 2013
Annals of Nursing and Practice
ISSN : 2379-9501
Launched : 2014
JSM Dentistry
ISSN : 2333-7133
Launched : 2013
Author Information X