Prior food level and temperature will affect age (and to a lesser extent size) at sexual maturity. Better fed fish will in general reach it earlier and at a larger size than poorly fed fish.
In the past I parametrized a Dynamic Energy Budget (DEB) model to zebrafish, Danio rerio (but this has been done for other species) and quantified the relationship expressed above for that species: i.e. range of possible ages and sizes at sexual maturity and how this relates to prior food history and temperature.
In the DEB framework that I used, the assumption is that "before sexual maturity the individual is developing, after that it no longer develops but allocates to reproduction".
In this framework, growth ( increase in length) is not the same thing as development, so after being able to produce offspring the individual can still grow.
Now the question I never fully resolved, is what exactly is sexual maturity and how to determine it with precision. It's not because the fish doesn't spawn or have mature oocytes that it is not sexually mature.
I was working under super controlled feeding conditions with a well studied model organism; how do we deal with less well known species and/or field data?
Bonjour Augustine,
This is a very interesting question. I thought much about it when I was working in aquaculture research. After reading the first half of your writing, I had an objection (what about environmental cues ???), but after that, you question yourself about this.
First, in reproduction, we do not often refer to "sexual maturity ". We prefer to use the term "puberty". It has two definitions. The first one, which is generally employed but I don't really agree with is when the fish produce "spawnable" gametes for the first time. Therefore, it corresponds more or less to the first spawning period. Myself, I prefer to refer to the time when fish is ABLE to produce "spawnable" gametes, which can be considered when fish is ABLE to START gametogenesis, provided that.adequate environmental cues are applied. This latter definition seems also to be your definition of "sexual maturity".
From my point of view, the DEB model suffers a major flaw in that it doesn't take into account environmental cues, which are of paramount importance, because they drive everything in fish. Of course, temperature is important for growth. But photoperiod is as much important and its effect with temperature is synergic. Regarding fish reproduction, it is even much more important. I will take the example of Eurasian perch, a species I know very well. As long as you maintain high temperature (20-24°C) and high photoperiod (>16L:8D), I observed that fish will never start gametogenesis for at least 3-4 years. And I'm pretty sure they won't reproduce in their whole life. Instead, they continue growing. However, at the age of less than one year old, you can induce gametogenesis, provided that you give adequate cues (decreases of temperature AND photoperiod). Therefore, in aquacultural conditions, one can say that puberty is reached at about 8-9 months in perch. This is something that also concerns other Percids and Moronids (sea bass and others).
In addition, in aquacultural conditions, fish growth can be observed, even during the reproductive cycle. It concerns mainly males, for which gametogenesis is not much energy consuming, compared to females. In the wild, it is of course another story, because of plenty of factors that strongly differ.
As a conclusion, I would say that DEB is mostly OK for tropical species like B. rerio that can trigger gametogenesis without environmental changes (although changes may trigger it sooner), but it does not apply in this state to temperate species, which all need environmental changes to start gametogenesis.
Well, these are only my thoughts and specialists might give you different answers.
In my opinion, it's fine to use the phrase "sexual maturation" to describe the physiological process from puberty to spawning. This is a complex, continuous process, including e.g. endogenous and exogenous vitellogenesis in females, and by looking at gonadal development, one can define stages of sexual maturation.
However, I find the phrase "sexual maturity" which the question concerns, a more difficult phrase to define or use. It implies that an individual fish, at some stage, "reaches sexual maturity". As sexual maturation is a process that normally ends with spawning, I feel that fish can only be termed to have reached "sexual maturity" just before spawning, when they have developed sperm and oocytes which can be fertilized. Earlier, they're still maturing.
Concerning energy allocation, weight and length growth during sexual maturation, I think this differs greatly among fish species, from those who stop feeding for extended periods prior to spawning and where energy is reallocated from somatic to gonadal tissues, to those who do not stop feeding/growing during sexual maturation.
I agree with you Bjorn. But to my opinion, Starrlight is speaking about puberty rather than maturation; i.e. the time when the fish is physiologically ready to start gametogenesis. This period corresponds in fact to the youngest age at which gametogenesis can occur and reach its end under adequate cues. This age must be determined experimentally because one has to check that gametogenesis ends with fertilizable gametes, as you pointed out. I would say these are retrospective experiments.
I believe your problem is not connected to the time of maturity, but, as already mentioned, which stimuli induce the zebrafish to produce gametes. One factor would be the presence of males and females in the same environment. It would be useful to research which stimuli (environmental, hormonal ...) that induce the reproducers of zebrafish to develop their gonads. I work with Neotropical fish species and are limited by environmental variations and the reproductive strategies of each species.
Thank you for these answers and the very interesting discussion- it has helped me clarify the question a lot; I guess my main question concerns the link between energetics and maturation. Maturation defined as all of the coordinated processes involved in developing. Puberty being the developmental stage when the individual is actually able to reproduce.
My conclusions/ thoughts for zebrafish are that it can take anywhere from 2 to 7 months to reach "puberty" and start spawning at 25°C; so potentially 5 months difference between individuals depending on their feeding history and imagining that there is no other special stress factor which modifies baseline eco-physiological performance. This potentially applies to all developmental milestones attained along the maturation gradient so to speak.
I agree with Bjorn, maturation is a continuous process, so puberty is not an instantaneous event. However, the thing with DEB theory is that energy/ mass allocation to maturity (before puberty) dissipates in the form of metabolic work involved with developing. After puberty allocation towards maturation stops and the energy/ mass gets stored in a buffer and used for reproduction. This makes 'puberty' a rather major event in terms of metabolism. I was looking for some empirical support for this....
A thought about Alexandre's comment: can the fish you are talking about completely delay developing their gonads till the right environment cue? Zebrafish do attain 'puberty' when fed correctly (and perhaps even pre-maturely when growth arrested for a long period in the early juvenile stage).
When they are able to produce mature oocytes- the wet mass of a female can increase by 30% overnight - the stimulus to produce mature ready to go oocytes is indeed environmental for this species and shows quite a bit of inter individual variability. The actual mass invested in reproduction at a given feeding level turns out to be much less variable. The major scatter in the signal seems to come from differences in stimulus for making ripe oocytes and energy density of a batch of eggs spawned.
I am agree with Neil Wang
i did a research on gonadal topic with Paraschistura nielseni. Multiple regression showed that body weight was closely related to the total weight, while no significant relationship was found between gonad weight and total weight. I think that reaching maturity in this species is not clear and there is a difference between "sexual maturity time" , "puberty time" and "spawnable time"
I agree and disagree with the conclusions drawn by different experts here, mainly in the context of aquaculture. The first spawning (release of effective spawanable gametes) that happens in the nature (environmental cues in balance) is not the same what happens in captivity. The fish of the same species might have different age of effective spawning (may not at all spawn in the captive cases..as it happened with the carps, shrimp). The basic driving factor is though the hormonal levels takeing part in the process of reproduction, other environmental stimulii might hinder or activate the process. Even for an intervened process of gamete maturation (the removal of maturation inhibition hormones in shrimp eye stalk is one example) or induction of spawning of mature oocytes (carp ovulation using hormonal injections such as OVAPRIM) there should be a basic readiness of the individuals to be responsive. Hence, I feel its the process of formation of fertilizable gametes that marks the begining of the sexual maturity.
As far as I know from other colleagues aquariologists, in zebrafish, thermal shock can induce spawning within a few days. These are however empirical observations. I wonder if photoperiod variations may also play a role. Sex ratio is probably important too, as pointed out by Alexandre.
Starrlight, thanks for your interesting explanation. Just, I don't understand this sentence at the end: "The major scatter in the signal seems to come from differences in stimulus for making ripe oocytes and energy density of a batch of eggs spawned."
What are the signal and stimulus you are referring to ?
Also, it's difficult for me to understand this definition: "Puberty being the developmental stage when the individual is actually able to reproduce."
You mean when gametes are ready to spawn ? Because if we strictly apply this definition, then temperate fish reach puberty every year and only for a short period. Otherwise, this may imply that the first reproductive cycle is particular, but why? Or do you mean something else ?
So I have a question for everyone because it was never clear to me: does the first reproductive cycle of fish have to be considered differently from the next ones? And if yes, why ?
Dear Neil,
By puberty I mean the capacity to produce ripe gametes. I consider the details about how/ when gametes ripen and when spawning is induced as needing to be specified separately and probably on a species specific basis. Unfortunately I do not have all of the answers to your questions. And will try and explain what I meant and how I think we might get some answers to those questions in the future.
In the past, I did mass balancing on individual female zebrafish for two different protocols.
Background: Zebrafish are continuous spawners; spawning and making ripe oocytes is strongly conditioned by food availability. If adult females are not with males they usually do not spawn. Very good papers give ideas on what induces formation of "ripe oocytes" in females. At the time is was thought it was stimulated by presence of a male, but there are also dominant females who might suppress this in other females ( see excellent work by Gerlach, Spence, and Lawrence)
Protocol 1: adult couples were kept continuously together for about 47 days
Protocol 2: males and females were kept separate for 20d and then put together to reproduce for about 15d (not my experiment, but same lab)
I was coming the the end of my project and had my zebrafish model which gives predictions for cumulative energy/ mass invested in reproduction which is estimated from the experimental curve of cumulative number of eggs produced. This was working quite nicely, but then I thought it would be useful to add some detail of not only what is invested in reproduction but also how many eggs released per spawn and what is the inter-spawn interval.
That is how I came to my first hypothesis: for zebrafish, the totality of what is invested in reproduction is not released in each spawning event; only part of what is invested into reproduction 'ripens' and makes ripe oocytes and then the individual spawns those ripe oocytes.
That is how I then defined 2 parameters:
- t0 (d) initiation of making the ripe oocytes and
- [EB0]: the energy desnity of ripe ooctyes which induces spawning (joules ripe oocytes/ volume of female structure). For a given amount of energy in an egg and size of the mother we have then the eggs/ spawn.
I was able to make rather remarkable predictions for inter-spawn interval and # eggs/ spawn for a given female zebrafish by finding value of t0 and EB0 for each female.
In protocol 2 I found out that t0 was initiated in three different instances depending on the female:
1- t0 must have started when the female was put with the male after the 20d of no reproduction
2 - t0 must have started sometime during the 20d separation phase
3 - t0 must already have been initiated before the experiment
Hypothesis: it is not only male pheromones which can triggers the oocyte ripening; maybe visual cue is enough.
During the 15d reproduction phase most of what was spawned even if t0 only started at the end of 20d was material invested since the beginning of the experiment. Thus the slope of the egg production during those 15d was relatively insensitive to the feeding during that time. The initial spawns were enormous. It seems that usually, perhaps not always, all the ripe oocytes are released in a spawn.
Protocol 2: During the 47d where couples were continuously together I initially thought that t0 must be initiated the whole time and then I only have to deal with how many eggs per spawn (EB0 parameter).
Then I was really surprised/ amazed to find out that since the individuals in the 47d experiment were very close to maximum size, small behavioural differences in ingestion meant that somatic maintenance costs were no longer paid- it seems that they routinely take from what was invested in reproduction and complete the payment of these somatic maintenance costs.
The new hypothesis I came up with when trying to fit the model to the data is that oocyte ripening is inhibited as soon as the individual starts to take from reproduction material to cover somatic maintenance costs.
However if there were ripe oocytes then these may or may not get spawned; I talked with some husbandry experts and they think that zebrafish are not efficient in resorbing the totally ripe oocytes but can more efficiently resorb the unripe material.
So to come back to your questions: the stimulus for producing ripe oocytes is quantified by what I call the t0 parameter and the choice 'to spawn or not to spawn' partly controlled by the [EB0] parameter.
This is my current thought status:
1 - the processes underlying initiation of t0 are still a mystery
2 - [EB0] shows a lot of scatter between individuals and probably depends a lot on husbandry (photoperiod, temperature, # individuals put together etc.).
If comparing across conditions with similar husbandry and wanting to test hypothesis on t0 and [EB0] then the major scatter will be a problem unless we can find out how much scatter is 'normal' and the distribution of that scatter.
The metabolism of the individual is less variable across individuals than [EB0] if ingestion is controlled. My prediction is that if one can master the controlled feeding then the cumulative energy invested into reproduction between healthy females of a same size (and carefully acclimatized) will show hardly any difference. differences will then hopefully mostly show up in the t0 and EB0 between the different females.
Under those conditions, we might be able to find out more about what triggers t0 and what processes control [EB0].
What I am saying relies on our ability to compute at all times the contribution of mass invested into reproduction to total biomass- that is why we need measurement of length, wet mass, ideas on intake + a fully parametrized DEB model.
.
Dear Starrlight,
Many thanks for your detailed explanation and sharing those really interesting results and thoughts with us. Just so we understand each other, let me introduce how I conceptualize fish life cycle. In brief, in female, development is as follow:
embryo --> larvum and phenotypical sexual differencation --> metamorphosis --> juvenile --> puberty acquisition --> recruitment from "undeveloped" oocytes --> vitellogenesis --> acquisition of final oocyte maturation (FOM) competence --> FOM (of which meiosis resumption) --> ovulation --> spawning.
What I call "undeveloped" is female at protoplasmic or early cortical alveoli stage. Sometimes late cortical alveoli can also be observed. But in any case, oocyte diameter is small.
Let's put aside the "embryo-->juvenile" period to begin with puberty acquisition (i.e. the ability to start oogenesis from “undeveloped” oocytes). As you already mentioned, puberty acquisition in fish is still a mystery. It seems that the couple kiss/GPR54 that control GnRH release is set up at puberty, as in mammals, but more research is needed to understand both external and internal determinism of its set-up. It is very probable that energetic state of fish play a role, especially in B. rerio. So perhaps your DEB model could contribute to unravel a part of this mystery?
Once vitellogenesis has started, we can have three type of gonad development, according to species:
- synchronous: all oocytes develop together at the same speed and have therefore always the same size and all are at the same developmental stage (salmonids)
- group-synchronous: same as synchronous except that a part of the oocyte stays at "undeveloped" stage (e.g. percids)
- asynchronous: all stages are encountered together in the gonad. This is the case of B. rerio.
Here, I have finished with definitions ;-)
To me, asynchronous development is the most difficult case to deal with, because clutches of different oocyte stage and size coexist within the gonad. Fish permanently recruit undeveloped oocyte clutches to undergo vitellogenesis, but also recruit vitellogenic clutch for FOM and spawning. In other words, you have vitellogenesis, FOM and spawning at the same time, which is not the case of synchronous and group-synchronous fishes. Moreover, since your species does not seem to rely on environmental variations to synchronize oogenesis, your females are not synchronized with each other. Am I right ?
So, I’m not totally sure of what you call “ripening”. Is it vitellogenesis, FOM or vitellogenesis+FOM? If it is FOM, t0 corresponds to the time when a vitellogenic clutch is recruited to undergo FOM and subsequent spawning. Note: FOM does not necessarily lead to spawning but can also lead to “overipening” or “overmaturation” and subsequent atresia. If “ripening” is vitellogenesis or vitellogenesis+FOM, then t0 corresponds to the time when an undeveloped clutch is recruited for vitellogenesis. I suppose that "ripening" mean "vitellogenesis+FOM” ?
In all cases, this however corroborates your hypothesis: ”That is how I came to my first hypothesis: for zebrafish, the totality of what is invested in reproduction is not released in each spawning event; only part of what is invested into reproduction 'ripens' and makes ripe oocytes and then the individual spawns those ripe oocytes.”
Indeed, during FOM, vitellogenesis continues in other oocytes and thus all energy invested in reproduction is not included within the FOMed and spawned clutch.
“It seems that usually, perhaps not always, all the ripe oocytes are released in a spawn.”
Yes. In most fish species, oocytes that have undergone FOM must be spawned within a few hours. Otherwise, they undergo “overripening”: oocytes proteins are too much hydrolised by internal enzymes and become atretic. However, vitellogenic oocytes can be stored for a much longer period. I think that we can suppose that in the absence of spawning cues, vitellogenic oocytes accumulate within the gonad with time, what could explain the big clutch of first spawning you observed in some females kept without males and suddenly coupled with them.
An interesting conclusion (among others) of your study as I understand it, is that t0 (puberty) do not depend on male presence, but spawning time does.
Thanks again for this interesting discussion !
Sexual maturity: Has to grow up to the certain age in a suitable environment and fish can desire to breed.or ready for mating with opposite sex. Female fish has enough abdominal enlarge and pectoral fin has enough lubricant naturally with mature egg and the male should have ripen milt for doing meet with female fish, they have nuptial color in morphology.. Both of the fish are ready for artificial breeding response.
Maybe you can detect attainment of sexual maturity, i.e., the first gonad ripening in virgin zebrafish by change in the length-weight ratio? There are several ways to do that. I used to test several years breakpoints in that relationship for detecting maturity attainment in brown trout and other salmonid fish which I was not to dissect (due to either they are considered pretious to anglers, or trully threatened).
In addition to what was said above in this thread, an attainment of maturity is related both to density (determining growth rate) and population structure (e.g., sex ratio, age structure) and other population parameters.
I hope this will help a bit.
Physiological definition of sexual maturity could be defined at the average/mean length at first maturity where the fishes in a population produces sufficient reproductive hormones to support response to environmental cues for reproduction and attainment of unhindered expression of sexual characteristics of the species.
Also physiologically the fish can be said to be sexually mature when there is a significant switch of energy allocation from somatic growth to development of gonads i.e. Sex cells and expression of sexual characteristics e.g. Colourations representative of the species.
Just to add some other thoughts here. There are many DEB approaches with different assumptions. You can have more flexible assignment to growth and reproduction/storage before maturation and you can include developmental or somatic growth after maturation also.... that is just a matter of assumptions. Different approaches are taken for different questions. In a population dynamics setting you would assume that if a fish has enough resources to reproduce, in a given year it will, so it is the environment experienced from birth to the time of maturation that sets the likelihood of successful reproduction in a given year. DEB models and variants of them are used by Andre de Roos at Amsterdam for modelling Eurasian perch and Baltic Cod and herring...have a look there and the references to DEB approaches therein
Dear Tom Cameron,
Thank you for these thoughts - I am very interested in the work done by Andre de Roos and co-authors on population dynamics. But my question referred not so much on how to implement different assumptions into DEB models but to what was going on in terms of the actual physiology of the fish ...
There are invasive and non invasive ways to go about measuring/ assessing whether or not the fish is sexually mature as I have learned from a number of very rich answers given above (see e.g. Neil Wang, Predrag Simonović, Azubuike Chukwuka ...).
The reason I bring this up is because if one wants to implement testable hypothesis on the fishes physiology then one needs to be on top of what the interpretation of a given set of observations are - several thinking steps/ assumptions are usually involved here. Looking back to the different answers, I have learned that there are several ways to measure if the fish is sexually mature or not - but do all of these responses relate to prior feeding and temperature in roughly the same way ? Do they all have the same error/ scatter structure ? Probably not, but there are (practical) reasons to choose one method over an other - hence the importance of the step of mapping data to model predictions and the role this plays in our interpretation of the world.
Hej
Well I agree. I just thought you stated only one such set of assumptions for your DEB and it seemed to me that it could be different. You probably know the work too, but also look at the work of Tara Marshall from Aberdeen who does quite a lot of research on maturation and growth strategies of north sea fish.
Other than that it seems you are looking at reproductive strategies. Although not on fish we have some done some work on this in invertebrates that have similar life histories to fish, in that fecundity is related to age and size at maturity. Here though, individuals are largely constrained to stop growing at maturity. See papers by Stewart Plaistow
and Tim Benton.
Best wishes
Tom
You can add some thoughts: Sexual maturity is attained when,
in males: spermatogenesis occurs
and in females: when germinal vesicle migrates to animal pole and oocytes hydrates
OK, I see that we all realize sexual maturity sligthly different, making a variety of explanations. Some speak about it thinking on the first year of reproducing, or attainment of maturity. Maturity itself, however, is the time when gonads are ripe, in their fifth stage of maturation, with the domination of spermatozoids and ripe ova in them, and with spontaneous (or almost spontaneous) leaking of roe and milt from the handled fishes in which gonads occupy almost the whole body cavity. Indicator for maturity such as Gonadosomatic Index GSI are invasive, but they are very precise in statistical sense, whereas other in the best case implicate to the change in the allocation of energy from somatic to the reproductive component (e.g., L-W relationship, growth rate, etc). I am not physiologist, but I am sure that aquaculture-oriented people are familiar with the level of hormones involved in the process of maturation and their ratio, so maybe that would be a clue for finding the answer on your question? This is the most direct physiological indicator of maturation I can imagine. Though, I assume that this sort of analysis on such small fish like Brachydanio rerio is very meticulous and demanding in technical sense.
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