Cephalopod Sex and Reproduction

Octopus researcher a sucker for hard work
Interesting new research but no paper yet.
Indeed Peter has been hard at work. The first paper from his PhD is out:

Morse, P., K.R. Zenger, M.I. McCormick, M.G. Meekan, & C.L. Huffard (2015) Nocturnal mating behaviour and dynamic male investment of copulation time in the southern blue-ringed octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae) Behaviour doi: 10.1163/1568539X-00003321 (28 pages)

If anyone would like to read it, send me your email address in a message, and I can pass along the pdf.
 
Male copulatory behavior interrupts Japanese flying squid Todarodes pacificus female spawning activity
Pandey Puneeta, Dharmamony Vijai, Jun Yamamoto, Yasunori Sakurai 2016 Marine Ecology Subscription

ABSTRACT: Batch spawning, intermittent spawning and multiple spawning represent common reproductive strategies among cephalopods. These flexible spawning strategies are also common in fishes, and are thought to be a female trait that is programmed depending on environmental parameters. The ommastrephid squid Todarodes pacificus, being a terminal spawner, is considered to have a single spawning event, extruding one large egg mass and dying soon thereafter. Females that are interrupted by males exhibiting mating behavior, while extruding the egg mass, spawn multiple egg masses over the course of 2-3 d instead of dying soon after spawning the first egg mass. We demonstrate that male mating behavior causes ‘forced’ intermittent spawning by females (i.e. more than one spawning event). We hypothesize that in T. pacificus, some males use this strategy to mate with females unable to repel advances while spawning, thus providing the male with the opportunity to contribute sperm and enhance gene flow.
 
Great octo sex talk!
Published on Jul 22, 2013
Dr. Janet Voight settles the eternal debate about the plural form of "octopus," and becomes my new favorite person.

Want more of Dr. Voight?! Check out her other videos and media appearances!
Podcasts
http://fieldmuseum.org/explore/multim...

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Expeditions
http://fieldmuseum.org/explore/past-r...

Partials - also see Field Revealed outtakes
http://fieldmuseum.org/explore/multim...
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Facebook: The Brain Scoop

The Brain Scoop is hosted and written by:
Emily Graslie

Created By:
Hank Green

Directed, Edited, and Scored by:
Michael Aranda

Assistant Editor:
Stefan Chin

Thanks to Martina Šafusová, Diana Raynes, Barbara Velazquez, Hervé Saint Raymond, Alex Austin, Tony Chu, John-Alan Pascoe, and Seth Bergenholtz for taking the time to transcribe this episode! WOOOOOO

 
Impact of cryptic female choice on insemination success: larger sized and longer copulating male squid ejaculate more, but females influence insemination success by removing spermatangia
Noriyosi Sato, Masa-aki Yoshida, akashi Kasugai 2016 (subscription Wiley)

Abstract
In polyandrous mating systems, sperm competition and cryptic female choice (CFC) are well recognised as post-copulatory evolutionary forces. However, it remains challenging to separate CFC from sperm competition and to estimate how much CFC influences insemination success because those processes usually occur inside the female's body. The Japanese pygmy squid, Idiosepius paradoxus, is an ideal species in which to separate CFC from sperm competition because sperm transfer by the male and sperm displacement by the female can be observed directly at an external location on the female's body. Here, we counted the number of spermatangia transferred to, removed from, and remaining on the female body during single copulation episodes. We measured behavioural and morphological characteristics of the male, such as duration of copulation and body size. Although males with larger body size and longer copulation time were capable of transferring larger amounts of sperm, females preferentially eliminated sperm from males with larger body size and shorter copulation time by spermatangia removal; thus, CFC could attenuate sperm precedence by larger males, whereas it reinforces sperm precedence by males with longer copulation time. Genetic paternity analysis revealed that fertilisation success for each male was correlated with remaining sperm volume which is adjusted by females after copulation.
 
What a night! Last night's dive was pretty exciting by ending with an octopus piggyback ride
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:wink: Octopus vulgaris (common octopus) has been known to use two mating positions. My previous mating videos have shown the distance position: male octopus at a distance extends his third right arm known as the hectocotylus (sex arm) into the opening in the female's mantle to place the sperm packet in the female's oviducal gland until eggs are fertilized. The second method of mating (shown in the video) is called mounting (looks like the octo is getting a piggyback ride haha). The male will leap upon the female and mount her mantle. Once he has mounted her, he will find the mantle opening with his sex arm. It usually only takes a few seconds for the sex arm to find the oviduct suggesting that there may be chemical cues involved.

I followed this mating pair for ~45min last night. Here are the highlights!


 
Chemical cues correlate with agonistic behaviour and female mate choice in the southern blue-ringed octopus, Hapalochlaena maculosa (Hoyle, 1883) (Cephalopoda: Octopodidae)
Peter Morse, Kyall R. Zenger, Mark I. McCormick, Mark G. Meekan, Christine L. Huffard 2016 (Oxford Journals subscription)

Abstract
Chemoreception cues potentially influence intraspecific interactions of cephalopods, including mate choice. However, at present there is limited empirical evidence demonstrating whether cephalopods can use olfaction to identify the sex or identity of conspecifics. This study examined the responses of the southern blue-ringed octopus, Hapalochlaena maculosa(Hoyle, 1883), to conspecific odours during controlled laboratory trials. The ventilation rates in aquaria of 25 wild-sourced animals were measured during four treatments: baseline, sea water, sea water containing male conspecific odour and sea water containing female conspecific odour. When used as ‘receivers’ in trials, female H. maculosa significantly increased their ventilation rates in response to male odours, but not to female odours. However, female response decreased significantly with the receiver's size during female-odour treatments. The ventilation rates of male H. maculosa were statistically similar in all treatments. However, their ventilation rates showed a significant progressive increase over the observation period during male and female-odour treatments. Eighteen of these animals (nine females and nine males) were used in focal-animal trials 1 week after odour-cue experiments. Of these individuals, females were significantly more receptive to copulation attempts, and spent significantly more time per day in copulation, with males whose odours had elicited a weaker ventilation response in prior trials. These results suggest that female H. maculosa can use chemosensory cues to discriminate the sex, and possibly identity, of conspecifics and that this information might influence their mate choice. However, the mechanisms underlying these responses and subsequent copulatory access to females by males remain unknown.

  • © The Author 2016. Published by Oxf
 
Egg Masses of Flying Squids (Cephalopoda: Ommastrephidae)
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Dharmamony Vijai 2016 (subscription BioOne)
ABSTRACT
Ommastrephid squids have a pelagic lifestyle, with reproductive behavior that is characterized by the extrusion of fragile, neutrally buoyant egg masses, the release of paralarvae into the surface plankton, and the use of large-scale current patterns for larval transport, leading to the assisted migration of populations. Although the exact process of egg mass formation is unknown, the most accepted hypothesis suggests that, at spawning, eggs are first coated with oviducal gland secretion and released with nidamental gland secretions. Subsequently, the eggs mix with broken spermatophores or spermatangia for fertilization. The fertilized eggs are then extruded into the seawater to form a globular mass. These neutrally buoyant gelatinous egg masses are thought to maintain their location in the water column by floating at the interface between water layers of slightly different densities (above the pycnocline). The embryos develop within a favorable temperature range. Once hatched, the paralarvae leave the egg mass and swim to the surface. This review assimilates and assesses all available literature on the egg masses of ommastrephid squids. The data presented here clearly show how fragmentary our knowledge is about this important reproductive stage. Thus, increased efforts are required to develop observation and sampling techniques in the wild to obtain more direct evidence about reproduction in squids.
 
Squid egg strategies

Published on Jun 25, 2014
Reproduction is one of the many challenges faced by deep-sea animals. In recent years, submersibles have allowed scientists to explore the lives of deep-sea animals in ways that were not possible before. One of the many exciting discoveries was that a mother of the deep-sea squid species Gonatus onyx broods her eggs by holding them in her arms, a behavior that had never been previously reported for squids. This shocking discovery was the first time scientists had evidence of parental care in squids. In 2012, a team of researchers led by Stephanie Bush, reported finding another species of deep-sea squid that broods eggs, Bathyteuthis berryi, suggesting that this form of parental care may be a common solution to a reproductive problem for deep-sea squids.

Publication:
Bush, S. L., Hoving, H. J. T., Huffard, C. L., Robison, B. R., & L. D. Zeidberg. 2012. Brooding and sperm storage by the deep-sea squid Bathyteuthis berryi (Cephalopoda: Decapodiformes). Journal of the Marine Biological Association of the United Kingdom. 92(7):1629-1636.

Video producer: Susan vonThun
Music: "Aqua lounge", www.freestockmusic.com
Script and narration: Stephanie Bush
Production support: Lonny Lundsten, Kyra Schlining, Nancy Jacobsen Stout, Linda Kuhnz, Bruce Robison

 
Single and multiple mating reduces longevity of female dumpling squid (Euprymna tasmanica)
Amanda M. Franklin, Devi Stuart-Fox 2017 (subscription Wiley)
Abstract
For many species, mating is a necessary yet costly activity. The costs involved can have an important influence on the evolution of life histories and senescence. Females of many species mate multiply and this behaviour can inflict a longevity cost. Most studies investigating the effects of multiple mating on female survival have been conducted on insects and the effects in other taxa are largely unknown. We investigate the effects of both a single mating and a second mating on longevity in female dumpling squid (Euprymna tasmanica), a species in which both sexes mate multiply. Through comparing the longevity of virgin, once-mated and twice-mated females, we found that a single mating reduced female lifespan by 15 days on average. A second mating resulted in an additional 8 day (on average) longevity cost, despite no difference in total clutch mass, number of clutches, single egg mass or number of eggs per clutch between once-mated and twice-mated females. This demonstrates a cost to multiple mating which may be independent of the cost of egg production. Furthermore, total clutch mass and female lifespan were positively correlated, whilst female lifespan decreased with increasing average water temperature. The presence of an additive effect of reproduction on longevity suggests that multiple mating in cephalopods may have benefits that outweigh these costs, or that there is a conflict in optimal mating frequency between males and females.
 
New Findings on the Behaviour of the Horned Octopus Eledone cirrhosa in Captivity
Marcos Regueira, Ángel Guerra, Ángel F. González 2017 (Thalassas: An International Journal of Marine Sciences subscription)
@sirreal - note the spontaneous spawning comment
Abstract
A total of sixteen individuals of horned octopus Eledone cirrhosa were caught using creels by a vessel of the small-scale fishery operating in the Ría of Vigo (NW Spain). Captures took place on the west side of the Cíes Islands (Galician Atlantic Islands Maritime-Terrestrial National Park) in March 2013 between 60 and 70 m depth. All the octopuses were females, ranging 355–950 g in body weight. Animals were kept alive and subsequently transferred to open seawater system. Observations under confined conditions resulted in several behavioural events, summarized as follows: i) visual attack sequence was described and found to be similar to that exhibited by Sepia sp., which involves three main phases: attention, positioning and seizure, ii) after a time of confinement, females spontaneously start to spawn in the artificial dens arranged inside the tanks, although eggs were unviable, and iii) females spawn within a shelter, inside which they remain during eggs development, and block the entrance with stones and other materials they find nearby the burrow. This behaviour has been observed for the first time in E. cirrhosa. These new findings are discussed and compared with previous literature.
 
Health status of post-spawning Octopus maya (Cephalopoda: Octopodidae) females from Yucatan Peninsula, Mexico
Katina Roumbedakis, Maité Mascaró, Maurício L. Martins, Pedro Gallardo, Carlos Rosas, Cristina Pascual 2017 (hydrobiologia subscription)
The present study aimed to evaluate the health status of Octopus mayafemales on different days after spawning (days 0, 10, 20, 30, and 40). A total of 25 O. maya females were examined in terms of physiological (i.e., weight loss, hepatosomatic and gonadosomatic indexes, and hemocyanin, protein, glucose, cholesterol, and acylglycerides concentrations in plasma) and immunological variables (i.e., total hemocyte count, hemagglutination, and phenoloxidase activity). We hypothesized that O. maya females should maintain their physiological integrity throughout the post-spawning period until the hatching of the offspring. Results showed that the physiological and immunological indicators measured in post-spawning females significantly changed with time. Loss of body weight over time and a decrease in the hepatosomatic and gonadosomatic indexes were observed. Hemolymph components showed variations that reflect the consumption of reserves and coincide with an increased immune process of hemagglutination and phenoloxidase activity in hemocytes. Our results demonstrate that O. maya females are adapted to maintain an adequate state of health to care for their spawn despite the long period of starvation and contribute to the identification of the mechanisms involved in maintaining the integrity of these animals during one of the most critical phases of their life cycle.
 
Multiple optic gland signaling pathways implicated in octopus maternal behaviors and death
Z. Yan Wang, Clifton W. Ragsdale
(subscription Journal of Experimental Biology 2018 : jeb.185751 doi: 10.1242/jeb.185751 Published 13 August 2018)

Editorial of study findings here:
The grim, final days of a mother octopus September 25, 2018, University of Chicago Medical Center


Abstract
Post-reproductive life in the female octopus is characterized by an extreme pattern of maternal care: the mother cares for her clutch of eggs without feeding until her death. These maternal behaviors are eradicated if the optic glands, the octopus analog of the vertebrate pituitary gland, are removed from brooding females. Despite the optic gland's importance in regulating maternal behavior, the molecular features underlying optic gland function are unknown. Here, we identify major signaling systems of the Octopus bimaculoides optic gland. Through behavioral analyses and transcriptome sequencing, we report that the optic gland undergoes remarkable molecular changes that coincide with transitions between behavioral stages. These include the dramatic up- and down-regulation of catecholamine, steroid, insulin, and feeding peptide pathways. Transcriptome analyses in other tissues demonstrate that these molecular changes are not generalized markers of senescence, but instead, specific features of the optic glands. Our study expands the classic optic gland-pituitary gland analogy and more specifically, it indicates that, rather than a single “self-destruct” hormone, the maternal optic glands employ multiple pathways as systemic hormonal signals of behavioral regulation.
 
How female squid inseminate their eggs with stored sperm
Yoko Iwata, Noriyosi Sato, Noritaka Hirohashi. Takashi Kasugai, Yoshiro Watanabe, Eiji Fujiwara 2019 (Current Biology subscription)

Summary
How sperm reach ova after mating is one of the central questions in reproductive biology. Many species copulate and store sperm in female reproductive organs until spawning [1]. The way females use stored sperm is closely associated with sperm competition and cryptic female choice. However, it is difficult to observe the process of fertilization in natural spawning, as fertilization usually occurs in some ‘hidden place’ within the female’s body. Here, we report the fertilization process of a squid using a glass plate as a spawning substratum, enabling observation within the female arm crown where the sperm storage organ is located and where fertilization may occur. Additionally, we detail the distribution of sperm around newly spawned eggs. Our observations reveal that: the female places her sperm-storage organ (seminal receptacle) over an egg held within her arm crown and inseminates the eggs one-by-one during attachment to the spawning substratum; sperm pass through a pathway within the jelly layers surrounding an egg; and such direct insemination behavior and the pathway through the egg jelly enables a female squid to externally fertilize her eggs using relatively few sperm. This study is the first to reveal the fertilization process using stored sperm, under female control.
 
Double Hectocotylization in Hubb's Octopus, Octopus hubbsorum(Cephalopoda: Octopodidae)
Mariana Díaz-Santana-Iturrios, Andrés Granados-Amores, Deivis Samuel Palacios-Salgado, Jasmín Granados-Amores 2019 (subscription BioOne)

Abstract
Double hectocotylization in octopods has only been reported for some individuals of a few species, often affecting arms of the same pair. We herein report several cases of non-bilateral double hectocotylization in a single species collected in different locations of the Mexican Pacific coast. The octopuses were identified by morphological and molecular criteria as Hubb's octopus, Octopus hubbsorum. The “regular” and “accessory” hectocotyli were examined by histological analysis; in the latter, the calamus was present and no ligula was detected. Double hectocotylization can be an intrinsic character of the species.
 

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