Very interesting question! During my PhD on waterbird-mediated dispersal I did not come across any published evidence on fish or fish eggs. However, to me it is evident that many more aquatic organisms are transported by waterbirds than we think, and I see no reason why fish eggs would not occasionally survive either internal or external transport when clinging to birds. It might be limited amounts per bird, but over time this can still add up and be "enough" for colonization.

- Even aquatic snails (gastropoda) can survive gut passage for many hours and are internally transported over large distances by waterbirds (see Van Leeuwen et al PLosOne). Some fish eggs may be just as tolerant.

- Aquatic snails will also cling to birds and can stay attached for up to 8 hours in mud (see Van Leeuwen et al Freshwater Science). Very likely sticky eggs of fish species that are desiccation tolerant enough can also, because anything attaches with mud. 

- A very large suite of aquatic organisms can survive passage through the digestive systems of birds because of a digestive trade-off in many birds (see review Van Leeuwen et al 2012 Jrl Biogeography). Why not fish eggs? We only know very little yet.

All the best,

Casper

Article Experimental Quantification of Long Distance Dispersal Poten...

Article Gut travellers: Internal dispersal of aquatic organisms by waterfowl

Article Prerequisites for flying snails: External transport potentia...

Good afternoon - yes a good question - most of the evidence is probably going to be anecdotal. I think that this is going to be such a rare and 'chaotic' phenomenon that designing an experiment to get 'proof' is probably not realistic.

I am in Canada and a local recently contacted me indicating that he has two similar artificial ponds on his property (they call then 'dugouts' here). With no possibility of connection to local surface waters and no natural waterbody as a start for the pit. He has noticed a healthy minnow population in one pond but not the other - I can think of no other way for the fish to get there other than the way you describe. The abundance of fish in this case is also of interest as it must be a breeding population and many of these systems freeze to the bottom here in the winter.

Also check publications from Andy Green @ Donana Biological Station,,

S

In response to Francois Massol - I not e that this dissertation chapter refers only to 'internal' transport of zooplankton - presumably in encysted forms. I believe the only viable form of transportation for fish eggs would have to be external ?

I grew up in the UK countryside. Along the lane where i lived was an old koi farmer. He specialized in albino grass carp. He had two large ponds, which he dug in the 60's, and personally stoked with juvenile trout and grass carp. Every autumn he would fish out some trout for the freezer. He told me that after 20 years, he one day fished out a 10lb common carp. The ponds are effectively in the middle of woodland, with no lakes near by and/or any way for a carp to get there aside from someone being kind enough to carry a carp though the woods for a couple of miles and throw in his pond, or as he firmly believed, by bird dispersal. I imagine its more common than we realize.

Hi Harald

There is growing evidence that freshwater fauna is transported externally by waterfowl although I do not remember finding papers on the transport of fish eggs. Latest experimental evidence reffer transport of adult amphipods and freshwater shrimp and even recently hatched crayfish juveniles. You can check the links to these papers:

Rachalewski, M., Banha, F., Grabowski, M. & Anastácio, P.M. (2013) Ectozoochory as a possible vector enhancing the spread of an alien amphipod Crangonyx pseudogracilis. Hydrobiologia, 717, 109-117.

http://www.springerlink.com/openurl.asp?genre=article&id=doi:10.1007/s10750-013-1577-7

Banha, F. and Anastácio, P.M. (2012). Waterbird-Mediated Passive Dispersal of River Shrimp Athyaephyra desmarestii. Hydrobiologia. 694(1): 197-204. http://www.springerlink.com/content/120n21133g011350/

Anastácio, P.M., Ferreira, M.P., Banha, F., Capinha, C., Rabaça, J.E. (2013) Waterbird-mediated passive dispersal is a viable process for crayfish (Procambarus clarkii). Aquatic Ecology.

http://link.springer.com/article/10.1007%2Fs10452-013-9461-0

cheers

Pedro Anastácio

The inland-most cenotes (karstic sinkholes) in the Yucatán have only two native fish species: Rhamdia guatemalensis, a scotophile catfish that could conceivable have arrived there by means of tunnels connecting the cenotes, and the guppy Gambusia yucatana. The catfish occurs in every cenote. The Gambusia occurs in many, but not all, with a somewhat erratic distribution: sometimes one cenote will have it, and another cenote nearby will not.

Now, Gambusia is a small poeciliid, a viviparous fish: in this case, the random dispersal that I invoke to explain this does not concern fish eggs and waterfowl, but rather adult fish and hurricanes: it could take just one gravid female to survive being airborne and blown from the coastal mangroves into a cenote to colonize the site. (So, not really answering your question, but I reckoned this would be an interesting marginal note.)

Hello Harald, This is an interesting one. I suspect that eggs that are tacky might adhere to the feet of waterfowl and so might become spread in this way. I have always wondered how brown trout will have invaded remote mountain lakes in Ireland. My explanation is that this might have been as a result of small tornadoes that will have carried eggs from a lower site and dropped these into a lake at altitude. These eggs lack a gas vesicle and so the changes in pressure with such a vortex are unlikely to result in trauma to the fertilised egg. In this case it needs only to happen once over geological time. We know so little about natural spreading modes of transmission and is an interesting study to fund but funding for such a study is unlikely to materialise.

I think there could be several reasons how fish comes to ponds. I assume that humans are very important in transplanting fish and that has been done for centuries. We have some isolated new made (last year) ponds for establishing a pool frog community, unfortunately in some ponds fish show up and they are predators. Fish are have been observed to migrate up in the ponds through "wet" grass quite long stretches.

Dr. Jordi Figuerola of the Estación Biológica de Doñana, CSIC. c/ Americo Vespucio s/n, 41092 Isla de la Cartuja (Sevilla) has studied bird dispersal of organisms and published widely on the subject. From his website "Most of my recent research focus on the factors that promote and limit dispersal of organisms in freshwater systems (including virus, bacteria, algae, plants and invertebrates) and the role of waterbirds in the dispersal of these organisms". I would look through his publications as they offer insights to this intriguing question.

Additionally to the dispersal of fish eggs on the feet and feathers of waterfowl or by tornado like weather events exists another intriguing possibility: The active stocking of juvenile fish by kingfisher species. On several occasions I observed kingfishers dropping fish in isolated water bodies in Southern Brazil. Although this contribution is not very scientific, it may be worth of reflecting…..

The Chinese/Amur sleeper (Perccottus glenii) is an alien species in Hungary but quite common. It spreads really fast along the River Tisza in the Danube water basin. It lives mainly in small ditches which are connected to the main channel BUT it occurs in isolated water bodies as well. These isolated marshes and fens are often in the middle of protected areas with no link to other water bodies nearby and the Chinese sleeper is the only species who lives in them.

There are no hurricanes in Hungary and this species can not crawl miles from one lake to an other so we can abandon these options. In addition these lakes are hardly visible from above and they are mostly covered totally with woody vegetation.

So my questions are:

1. If the species is introduced to these habitats by waterfowl how can they notice these wetlands?

2. Why mostly only one species is introduced to these habitats? You have mentioned e.g. carp, minnow in your examples but no others. I think there have to be others who can "travel" this way especially if the "donor" habitat has more than one fish species.

Roland, this is a most interesting study and it just shows how little we know on dispersal mechanisms. I presume that anthropogenic transmission is unlikely, in which case it make it all the more interesting. I would presume that the movement would be of the fertilised eggs and if this is the case are these resistant to desiccation I wonder? I have noted Potamopyrgus antipodarum in puddles in large numbers on an occasionally used road, just in some puddles. Birds frequent the area but car tyres might also be responsible or mud clogs falling from dirt infested cars.

I found a very interesting abstract in this topic.

A Hungarian student conducted a research with ducks and with crucian and prussian carp eggs. He fed ducks with duckweed (carp eggs attached to the plants) or fed the ducks directly with eggs. He found living eggs in the faces in both cases but only in few number. The eggs were in good condition and healthy fries hatched from them. In addition they became fertile adults.

Briefly, I think waterfowl can introduce fishes to new habitats in two ways: with faces from "above" while they fly or eggs attached to their feather. The first option could be the answer for my previous questions.

Hi Roland, can you provide the reference to this work. Most interesting. Any information about the egg membrane which may help to deduce if this may happen for other species. I presume it will be small eggs that would be most likely to survive such conditions or those that might survive aerial exposure. Any ideas?

Dear Dan,

I found this information in a Hungarian abstract book of a workshop. The author was a student of an other universtiy and I couldn't contact him yet. I didn't find an article either. The abstact contains only a few informations but nothing about the membrane or the size of the eggs.

New info that the eggs were split into two groups for the experiment. The first group was the control, the other was treated to remove the stickiness of the eggs. The ducks were fed with both type of eggs - the treated eggs directly with Pasteur pipette, the "control" eggs were attached to Lemna minor. Both eggs contained living embryo after digestion which lasted about 0,5-1,5 hours.

I am really interested in this topic so if I will get a new information I will share it with you.

Many thanks Roland. Yes I would be interested like you. I am interested in natural dispersal processes..

Hi All,

I just came across this discussion and was intrigued enough to finally give in and set up a research gate account. I am currently preparing a manuscript on the contentious issue of the crucian carp's (c.carassius not c.auratus as the Chinese call it) status in England, i.e. native or introduced. My genetic evidence points to them being introduced here very recently by humans. However in the back of my mind I have the idea that maybe, as you discuss above, eggs could have been bought here on the feet of waterfowl. In my mind this is almost an impossibility - however I was interested to know if anyone tracked down that Hungarian student, who's abstract eludes to this in crucian carp.  

Any info would be really useful.

Cheers

Dan

Hi all,

In 1950 A. Thienmann published his „Verbreitungsgeschichte der Süßwassertierwelt Europas“. On page 156 he gives a chapter on „Transport of aquatic animals by birds“. I found an English translation of this German text by Nock P.L. (F.B.A. Translation No. 57). Find it attached. It is interesting, but more interesting I find the paper he is citing: Schiemenz F. 1925. Fish egg resistance against air transport (in German).

In this paper another paper is cited: Preuße O. 1925. How do fish disperse. II. (In German). The author mentions that he found fish eggs in duck faces. A few days later fry of Esox lucius hatched from them. I have the impression that this is a kind of natural dispersal virtually not considered but possibly very important. If needed I can prepare English summaries of both articles.

Best,

Harald

Hi Harald,

Interesting account.  I have often wondered how trout managed to colonise upland lakes.  The transmission by birds is one possibility but how about fertilised eggs being transmitted by waterspouts?

Would be interested in the translation you suggested you may have time to do

all the best

Dan

Very interesting question! During my PhD on waterbird-mediated dispersal I did not come across any published evidence on fish or fish eggs. However, to me it is evident that many more aquatic organisms are transported by waterbirds than we think, and I see no reason why fish eggs would not occasionally survive either internal or external transport when clinging to birds. It might be limited amounts per bird, but over time this can still add up and be "enough" for colonization.

- Even aquatic snails (gastropoda) can survive gut passage for many hours and are internally transported over large distances by waterbirds (see Van Leeuwen et al PLosOne). Some fish eggs may be just as tolerant.

- Aquatic snails will also cling to birds and can stay attached for up to 8 hours in mud (see Van Leeuwen et al Freshwater Science). Very likely sticky eggs of fish species that are desiccation tolerant enough can also, because anything attaches with mud. 

- A very large suite of aquatic organisms can survive passage through the digestive systems of birds because of a digestive trade-off in many birds (see review Van Leeuwen et al 2012 Jrl Biogeography). Why not fish eggs? We only know very little yet.

All the best,

Casper

Article Experimental Quantification of Long Distance Dispersal Poten...

Article Gut travellers: Internal dispersal of aquatic organisms by waterfowl

Article Prerequisites for flying snails: External transport potentia...

Hi Harald,

I have seen plenty of paper regarding aquatic invertebrates including some of Caspers and these couple, but I haven't found any with regard to fish eggs. I also tend to agree with caspers though that it is possible.

Cheers

Pete

Figuerola & Green 2002 Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshwater Biology, 47: 483-494.

Frisch et al. 2007 High dispersal capacity of a broad spectrum of aquatic invertebrates by waterbirds. Aquatic Sciences, 69: 568-574.

That´s just amazing. And unfortunately I´ve never found any publication mentioning this for fishes. In Brazil we have the Hoplias malabaricus fish, commonly found in isolated ponds. Many say that birds carry ´em but, till now, I haven´t found any article.

Hello Harald

while salmonid eggs are smooth, many other fish eggs are sticky, using this property to adhere to water-weeds. T\I believe they could therefore adhere to birds, or to weeds being transported by birds.

Best wishes, Julian

While certainly not 'proof,' Spencer and Patchett (1997) call on bird-mediated transport of mollusks to explain marine/estuarine species in what they infer to be ~5 Myr non-marine deposits (references therein on page 774 may be of service). 

I've been in a couple of debates over this.  I believe one possibility to consider in the Eastern U.S. would be the potential of fish eggs being transported by snapping turtles as they travel from one water body to the next.  

I think the fish-egg dispersal-by-birds issue is really IMPORTANT and should be better investigated. It may help explain some distribution patterns (some species of fish on islands, e.g. Aphanius fasciatus at three localities Cyprus, despite the fact that total dessication events have probably taken place many times - and the re-colonization is difficult there). So,... many thanks to Harald for bringing this up and providing that wonderful translation by the great August Friedrich Thienemann.  

Also I would like to add a story from Wikipedia about the Leucaspius delineatus, the Sunbleak, which as a telling german name..."The common German name Moderlieschen.  Literally meaning "the little motherless one", this ultimately refers to the fact that the sticky eggs of the moderlieschen can withstand exposure to air for a remarkably long time. Deposited on water plants, they sometimes stick to the feet of ducks and similar birds and are carried by these to ephemeral ponds. Large numbers of young moderlieschens are thus sometimes encountered when such ponds dry up, and with no adult fish being present this gave rise to the belief that they were "motherless".

Logically. I think it could be, because some fish find in some place that could not be explained how they are there.

There is a good review paper on the scarce literature concercing fish egg transport by water fowl by B. R. Schmidt 2013 (in German, but with an English summary).  He comes to the conclusion that in rare cases pike eggs might be transferred by ducks to a fish-free pond, however in most cases anthropogenic fish transfer seems to be the most likely reason. Furthermore, he refers to another review by Green & Elmberg (2013). 

Article Ecosystem Services Provided by Waterbirds

Article Transportieren Enten Fische in natürlicherweise fischfreie A...

Susanne Böll already mentioned the review paper that I published some time ago. When I reviewed the literature, I did not find convincing evidence for the transport of fish eggs by ducks. Ducks transport all kinds of other stuff and this is well documented.

This is a wonderful question. I could say that probability it could happens but it would be rare surely. I have down research for distribution of Baetis sp.how they are exist in down stream while there is barrier to move from up to downstream.

I often give talks about codispersal by waterbirds and "do fish get dispersed by birds?" is easily the most frequent question I get asked. There is much speculation about this process, including by Wallace, but no hard evidence to my knowledge. Epizoochory of fish eggs resistant to desiccation seems the most likely mechanism. Fish-eating birds that drop  live prey when in flight may also help spread fish between neighbouring lakes. But I think we often underestimate the extent of flooding during extreme events, so when we wonder how fish reached places this is probably usually the cause. Here's an interesting paper "The results show that rainbowfish eggs could readily be transported between catchments by aquatic birds....":

Oulton, L., Carbia, P. & Brown, C. (2013) Hatching success of rainbowfish eggs following exposure to air. Australian Journal of Zoology, 61, 395-398.

I haven't read the Oulton et al. paper but it seems to fit the typical pattern. They provide evidence that one part of the transport process may work (hatching after exposure to air) and then make a conclusion that is not supported by the data (eggs could readily be transported).

In many cases, transport by humans is way more likely.

COPP, G. H., K. J. WESLEY & L. VILIZZI (2005): Pathways of ornamental and aquarium fish introductions into urban ponds of Epping Forest (London, England): the human vector. Journal of Applied Ichthyology 21: 263-274.

COPP, G. H., L. VILIZZI & R. E. GOZLAN (2010): The demography of introduction pathways, propagule pressure and occurrences of non-native freshwater fish in England. Aquatic Conservation 20: 595-601.

Perhaps storms move more fish than birds as suggested in this Science paper: Bajkov A.D. (1949). Do Fish Fall from the Sky. Science, 109, 402-402.

I just came across this paper that doesn't mention birds, but is clearly relevant Hirsch P.E., et al. (2016). A tough egg to crack: recreational boats as vectors for invasive goby eggs and transdisciplinary management approaches. Ecol Evol, 6, 707-715.

Hi Harald,

Here se provided some exemples with zooplankton. We believe that some man native fish can be transported with water. Please see below.

https://www.researchgate.net/publication/316487742_The_small_foreigner_New_laws_will_promote_the_introduction_of_non-native_zooplankton_in_Brazilian_aquatic_environments?_iepl%5BviewId%5D=00RCZOwfpysjcAlYBUMYTZioGa1lQ2Q7BnR8&_iepl%5Bcontexts%5D%5B0%5D=prfhpi&_iepl%5Bdata%5D%5BstandardItemCount%5D=2&_iepl%5Bdata%5D%5BuserSelectedItemCount%5D=0&_iepl%5Bdata%5D%5BtopHighlightCount%5D=2&_iepl%5Bdata%5D%5BtopHighlightIndex%5D=1&_iepl%5Bdata%5D%5BfeaturedItem1of2%5D=1&_iepl%5BtargetEntityId%5D=PB%3A316487742&_iepl%5BinteractionType%5D=publicationTitle

Hi all,

adding to the list but not really solving the issue entirely is this article we just had out.

Colonizing Islands of water on dry land—on the passive dispersal of fish eggs by birds

http://onlinelibrary.wiley.com/doi/10.1111/faf.12270/full

It seems that there is hardly and empirical evidence for birds translocating fish eggs. That said, absence of evidence is not evidence of absence.

Nice. When I reviewed the literature, I also found that there is no evidence for the dispersal of fish eggs by waterbirds:

http://www.zora.uzh.ch/id/eprint/81606/

Well some eggs are sticky and wading birds might spread the eggs that might become attached to their legs. I think Pseudorasbora might be such a case and worth following up.

I think whether a study is worthwhile really depends on the goals. If you want to understand why there are fish in isolated ponds where you don't expect them, then it is probably easier to look for introduction by humans. There is plenty of evidence that humans release fish in all kinds of waterbodies.

If your goal is to document an interesting dispersal pathway, then it will be challenging to exclude other ways of colonization (primarily introduction by humans).

Thanks for the interesting discussions. I am interested ("informally" as I do not study the species only breed in aquarium) in Leucaspius delineates. Old literature, intuition based, refers to egg carrying by birds. But I do not find scientific evidence for this. So, it remains speculation for this species, based on what I read.

We recently went through the literature on species transport as related to pupfish in eastern California.

Sorry for the incomplete answer. We found abundant literature, going back to Darwin, of invertebrate transport by birds. We did not find any documented studies of vertebrate transport. One of the papers we found helpful was Reynolds et al., which I didn't see in the discussion thread. Humans are the likely movers of fish in some cases, but otherwise the isolated fish in eastern California represent isolation over millions of years and the dispersal mechanism was by Miocene-Pliocene interconnected rivers and lakes.

The Wikipedia article on biogeography provides a good summary of the history and status of the field. https://en.wikipedia.org/wiki/Biogeography

This issue was briefly raised by Chimits (1956) (in French). He stated that it is impossible for water birds to transport the eggs of pike, because this fish was was absent in a watercoarse 13 km away from a water with pike. An interesting argument.

Congratulations! This is interesting. It looks as if you showed that there is a mechanism. Did you also show how frequently it happens? If it *can* happen, then this does not mean that it is a common phenomenon.

Hey Giliandro G Silva ,

unfortunately I can't find this accepted manuscript. Is it online already? Could you please provide a link or a proper reference. Thanks in advance.

It is not online yet, we are expected it to be so anytime soon...

Here it is

https://esajournals.onlinelibrary.wiley.com/doi/10.1002/ecy.2774

Yes, now it is online!

Article Killifish eggs can disperse via gut passage through waterfowl

CHECK THIS: Killifish eggs can disperse via gut passage through waterfowl

This is quite an amazing result! However, it shows that fish eggs can survive and hatch. Dispersal may occur but has not yet been shown. It is also unclear how common the process is.

Well, eggs of some fishes are extremely durable and can survive outside water for days or weeks or even months, e.g. the annual killifish. When traveling desert areas in Brazil I was amazed about the distribution of annual killifish species over a fairly wide stretch and often really spotty. Even remote waters which hardly ever will be flooded by a river contain killifish. Water fowl in my mind most probably is part of this distribution process.