Captive Breeding Negatively Impacts Reproductive Success in the Wild

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I bred parrots and other birds for zoos and for the pet trade for years before I moved to NYC. I often thought about applying my avicultural and ornithological skills and talents to propagate birds for release into the wild, to supplement wild populations that are decreasing. But in addition to the practical challenges of captive breeding birds, I often wondered about the evolutionary implications of doing this: because every individual is precious in a captive breeding program, they are subjected to relaxed natural selection criteria, so would I be raising birds that were less fit? If so, could captive breeding potentially damage the very wild population that it is intended to help?

Last week, a paper was published in Science that addresses some of my concerns. This paper, which focused on salmonids instead of birds, was published by a group led by Hitoshi Araki, a zoologist at Oregon State University (OSU) in Corvallis, studied local hatchery programs that are intended to enhance threatened populations of Pacific salmon and steelhead trout on the west coast of the United States.

Every year, hatcheries release in excess of five billion juvenile salmonids into the North Pacific Ocean, both for anglers to catch and also to replenish diminishing wild populations. But these numbers also provide a huge dataset for researchers to study. Previously, researchers found that when hatcheries rely on captive-reared fish for their broodstock over many generations, their fish populations develop a distinct gene pool due to the effects of reproductive isolation and genetic drift. But curiously, one study noted that even hatcheries that rely on local wild fish for their broodstock end up producing captive-reared fish that are genetically distinct from wild populations. Is there an evolutionary significance to this genetic difference? Does this genetic difference negatively affect reproductive success in captive-reared fish?

In spite of some early research by Araki (in conjunction with another group) which suggested that the reproductive success of first-generation captive-reared fish might be indistinguishable from that of wild fish, Araki wanted to better understand the genetic effects of captive breeding on the reproductive success of captive-reared fish in the wild. To do this, Araki's OSU team designed an experiment where they compared the percentage of offspring produced by each of two pairings for captive-reared fish (C) that were born in the same year, raised in the same hatchery and released at the same time, as follows;

  • captive-reared fish produced by two wild-born parents (C[WxW]) or
  • captive-reared fish produced by a wild-born parent and a first-generation captive-reared parent (C[CxW])

Araki's estimated the reproductive success for 547 C[CxW] and 193 C[WxW] fish collected from three salmonid "run years"; when adult fish return to their natal rivers from the ocean to spawn. Using DNA fingerprinting, the team established the parentage of 355 wild-born returning salmon as having either one C[CxW] or C[WxW] parent. Based on these data, Araki's team found that the reproductive success for C[CxW] salmon was only 55% of that for C[WxW] salmon.

Amazingly, this study found that reproductive success declined sharply after a short time in captivity (figure 2a, below);

When a meta-analysis was performed comparing this study's data to previously published data, they all described a remarkably fast decline in reproductive fitness associated with captive-breeding: there was a 37.5% decrease in productivity after just one generation in captivity (figure 2b, above).

The evolutionary mechanism underlying this reproductive decline is unknown, but I'd be willing to bet that relaxed natural selection criteria are playing a strong role, which also would alter the resulting gene pool without increasing the overall mutational load.

I find these data to be alarming. Do these data reflect what is happening for other vertebrates, such as birds and mammals? Based on my own experience and knowledge, I would not be surprised to learn that there are sharp declines in reproductive success for captive-bred and -reared birds that have been released into the wild, just as there are for these fish. Further, because birds have a long learning/imprinting period (unlike fish), I suspect that the effects of captive breeding on wild avian populations would be more profoundly damaging, and those damages would extend beyond genetics to include behavioral and cultural effects. I think that Araki's team's study has important and potentially far-reaching implications for captive-breeding programs.

Source

"Genetic Effects of Captive Breeding Cause a Rapid, Cumulative Fitness Decline in the Wild" by Hitoshi Araki, Becky Cooper, Michael S. Blouin. Science 318:100-103 (5 October 2007 | DOI: 10.1126/science.1145621) [PDF]. (images, quotes)

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Does it really matter? Isn't the point to preserve the species? If so then dumping less fit members in the wild serves the same goal. Ensure that the raw numbers are there and let natural selection do the cleanup work.

Troy - the problem is that you'll lose the variation that fitness can act on, and in particular the phenotypes that are fitter in the wild.

Bob

So which is better - a less genetically varied but surviving species, or a highly varied and extinct one?

Bob,

Its all academic if the species goes extinct. Besides the variability is something that will arise again naturally, Parrots wont.

This is one of the reasons why freshwater fish stocking programs are a disaster, and don't accomplish the stated goal of increasing the fish population.

The bad numbers on freshwater fishery stocking programs didn't have a good explanation until the genetics got worked out. People in the upper Midwest, who depend on fishing as a source of tourism, didn't want to believe that dumping fingerlings in the local lakes was not going to solve the problem of declining sport fish populations.

I'm half with Troy here, in that for some species, (like salmonids) the damage done by captive breeding might well be countered by later selection. The catch is that as he notes, you'll need "raw numbers" for that. (If, say, you've got a 37% penalty, you can release twice or three times as many.)

The problem is, that's just not going to work for a whole lot of species, because there are issues that can produce 100% mortality, with little warning or recourse!

For starters, if you oversaturate their niche, that can not only kill off any surviving wild-types, but knock their food supplies down to unrecoverable levels, and otherwise degrade their environment. Similarly, the crowding can cause a boom for predators, parasites, and disease, which may hurt other species as well.

As GS notes, many species have "personal state" as well -- individual animals need some mixture of imprinting, modeling, and/or parental teaching. Without that, or with inferior human imitations, they may be unable to hunt or forage, to evade predators and other hazards, to court, mate and raise young, and/or to form functional social groups.

The details of what's needed can vary not only by species, but according to the details of their release area -- what's good to eat, and where/when can it be found, which areas are safe from predators or pests, what resources might help them to get at the former while avoiding the latter, and so on....

Then too, some of the smarter species may not want to leave their sheltered lab with its guaranteed food supply -- and a few of them may be able to find and come back to said lab, which would at least be fairly embarrassing....

By David Harmon (not verified) on 13 Oct 2007 #permalink

"Do these data reflect what is happening for other vertebrates, such as birds and mammals? Based on my own experience and knowledge, I would not be surprised to learn that there are sharp declines in reproductive success for captive-bred and -reared birds that have been released into the wild, just as there are for these fish. Further, because birds have a long learning/imprinting period (unlike fish), I suspect that the effects of captive breeding on wild avian populations would be more profoundly damaging, and those damages would extend beyond genetics to include behavioral and cultural effects. I think that Araki's team's study has important and potentially far-reaching implications for captive-breeding programs."

I expect that the effect occurs with all species (us included), but the percentage differs from species to species and captive raising to captive raising.

One major difference between most fish and essentially all birds is that most fish (salmonids among them) have lots and lots of offspring, with only a few surviving to reproduce. Birds typically have far less offspring over their lifespan, and a much higher percentage of their offspring survive to reproduce. Thus I would expect the 'mortality due to captive raising' to be much lower with birds because captive raising does not increase the number of 'survivors to age X'
as much.

Salmonids and other fish do some imprinting and learning, although birds typically do a whole lot more. The effects of losing culture probably depends on what roles culture serves in that species. Humans without culture are crafty, but probably not fully sane, apes. We simply are not able to be 'whole animals' without some sort of culture, but I'm not sure that culture is as intrinsically necessary for birds...perhaps for most birds their cultures are a consequence of their intelligence, but not necessary for having their level/sort of intelligence. If (_if_) this is so it might be that many species of birds can survive without/adequately recreate culture in a generation or three.

Still, even if all of the above suppositions are applicable and accurate I would expect there to be increased mortality among almost all captive-bred animals when they are released in the wild - if not (due to continued human intervention) in the first generation then almost certainly in the second generation.

Additionally, even _if_ birds can still manage to prosper after losing culture it still seems pretty darn sucky that they are in a situation of losing that culture in the first place. It may be a rather rudimentary culture, but any culture is, in part, an aesthetic and artistic creation whose loss is a loss to all thinking beings. (Given some of the nasty things humans have done to each other for cultural reasons I'm perfectly willing to say that some cultures should only 'exist' in books, but they should still not be forgotten.)

By Christopher Gwyn (not verified) on 13 Oct 2007 #permalink

Its all academic if the species goes extinct.

True. So why waste a lot of money doing something that won't work? Conservation works to a tight budget.

Besides the variability is something that will arise again naturally, Parrots wont.

Are you aware of how long it would take for genetic variability to return? Typically in captive breeding populations, we're starting from a small base population (i.e. little variation), and the breeding will reduce that further.

When the species is returned to the wild, typically only a few individuals are released (salmonids are atypical in this regard), so there isn't the variation in the population, and it's only going to enter the population through mutation, which is a slow process. By that time, the population will have been through several bad years, epidemics etc., which can wipe it out. Basically, the time scale over which variation is replenished is too long, as compared to the time scale of population dynamics, which is where extinctions occur.

Bob

This study confirms what has been long known in fisheries biology, captive bred animals are not nearly as able to survive as wild bred populations.

An analogy with birds is the thick billed parrot, which lives in southern Arizona and northern Mexico. Captive bred birds were released into the the wild and quickly died because they were not adapted to life in the wild.

Sciencegrrl have you been to the Queens Zoo which has a exhibit where they are breeding thick billed parrots?

i have not been to the Queens Zoo, although i have seen thick-billed parrots at the San Diego Zoo several times now.

incidentally, don't get me wrong here. i am a strong supporter of captive-breeding programs for birds BUT i also recognize that the goal for pcative breeding is to preserve the wild population, NOT to make the wild animals dependent upon humans to maintain their population numbers.

there are many things about this study that concern me, not the least of which is the suggestion that, by releasing captive-bred animals into the wild knowing that they have a signficant reduction in reproductive success (even when they mate with a wild-reared animal), the reproductive "penalty" is increasingly felt throughout the entire wild population until the population's ability to maintain itself in the wild has completely collapsed.

THAT concerns me. the source of THAT problem MUST be identified and then it MUST be addressed before we muck around with more and more populations of wild animals, potentially damaging them and their gene pools until they cannot recover regardless of what we do to "help" them.

Can of worms like no other... I've been following the last ~8 years of Attwater's Prairie Chicken drama and it's not pretty. The wild population just keeps dropping and the released critters that are supposed to supplement the wild ones just keep getting eaten. Captive birds have essentially 0 instinct and according to some paperwork I came across in '03, the average life span of a released bird in spring was 123 days. Average life span of a released bird in summer/fall was 23 days. It's a matter of geography for that site due to fall raptor migration, but how sad is it that these birds never even make it to the gene pool? Or is it? The wild birds can barely hang on regardless.