Manna Warburton & Gerry Closs Downstream Spawning Migration in Amphidromous Fishes: A Link to Catadromy through Larval Transport Manna Warburton & Gerry Closs Dept. of Zoology, University of Otago New Zealand Torrentfish Mike Joy G. brevipinnis Stella McQueen G. huttoni Hi everyone, my name’s Manna Warburton and I’m going to be presenting some work I did with Gerry Closs form the University of Otago, and I’m going to be talking about how downstream spawning migrations in amphidromous fishes form a link to catadromy through larval transport. Bruno David

Amphidromy & Catadromy Both diadromous life history strategies Diverse range of taxa Gobiidae, Cottidae, Galaxiiidae, Eleotridae, Prototroctes, Pinguipedidae, Retropinnidae, Kuhliidae, Bovichthyidae Widespread geographical distribution Indo-Pacific & Caribbean coastlines & islands Typically (but not exclusively) Relatively small species High fecundity, with small eggs Obligate pelagic larval stage Before I get into it, I assume you’re all familiar with the form of diadromy that’s common in the northern hemisphere, which is anadromy, which is practiced by salmonids. Amphidromy and catadromy are the other two forms of diadromy, and they include a wide range of taxa and are common across much of the southern hemisphere, and are typically but not exclusively small bodied fish with high fecundity and an obligate pelagic larval stage.

Amphidromy & Catadromy Fresh Water Sea Growth to adult Pelagic larvae Weeks to months Post-larval to Juvenile Migration Larval Migration Spawning & rapid hatch Adult Amphidromy Fresh Water Sea Growth to adult Spawning Adult migration to sea Pelagic larvae Weeks to months Post-larval to Juvenile Migration In amphidromous life histories, adults live and spawn in fresh water, and larvae undergo a rapid migration into the pelagic marine environment where they live and grow for some time before returning to freshwater to complete the lifecycle. Adult Catadromy

Amphidromy & Catadromy Fresh Water Sea Growth to adult Pelagic larvae Weeks to months Post-larval to Juvenile Migration Larval Migration Spawning & rapid hatch Adult Amphidromy Key difference Fresh Water Sea Growth to adult Spawning Adult migration to sea Pelagic larvae Weeks to months Post-larval to Juvenile Migration Catadromous life histories differ only in that adults perform a migration into the marine environment before spawning, with the other elements of the lifecycle being the same as amphidromous life histories Adult Catadromy

Amphidromy & Catadromy Fresh Water Sea Growth to adult Pelagic larvae Weeks to months Post-larval to Juvenile Migration Larval Migration Spawning & rapid hatch Adult Amphidromy Near-catadromous Mildly catadromous Quasi-catadromous Fresh Water Sea Growth to adult Spawning Adult migration to sea Pelagic larvae Weeks to months Post-larval to Juvenile Migration As more information has been collected about migratory behaviours, a suite of amphidromous fishes that perform downstream migrations prior to spawning has created some confusion about what category they belong in, and they’ve been referred to in the literature as “near catadromous” mildly catadromous and quasi-catadromous, so there’s some confusion about where they belong. Adult Catadromy

Why Amphidromy or Catadromy? Gross Proposed amphidromy transitional between anadromy & catadromy Anadromy & catadromy transitional between marine & freshwater life histories Direction of evolution related to relative productivity of marine & freshwater habitats McDowall Didn’t really consider catadromy extensively Argued amphidromous life histories allow larval dispersal to new habitat So why be amphidromous or catadromous for that matter? Why engage in migrations between freshwater and marine environments at a sensitive stage of development? Well Gross attempted to answer this is 1987 when he proposed that amphidromy was a transitional state between the other two diadromous life histories. He went on to postulate that anadromy and catadromy were themselves transitional states between non migratory marine and freshwater life histories, and that the direction of evolution was related to the relative productivity of the environments these animals were migrating between. Bob McDowall, who is widely considered to be the father of amphidromous research in the southern hemisphere, argued that amphidromous life histories specifically allowed for dispersal into new habitats in species that lived in very isolated freshwater streams on tropical islands Gross (1987) Am Fish Soc Symp; McDowall (2007) Fish & Fisheries

An Alternate View of Amphidromy (& Catadromy) Closs, Hicks & Jellyman A life history strategy that allows for high fecundity in (mostly) small fluvial fish species Produce tiny larvae that must rear in pelagic environment, usually marine Consequently, a life history restricted to species that can rapidly transport eggs or larvae to sea Dispersal is an incidental but useful ‘by-product’ Small eggs allow for high fecundity But limited resources (yolk) for larvae Must rapidly complete migration from stream to sea before starvation occurs So this year, Closs Hicks and Jellyman proposed an alternative explanation for the role of amphidromy, and I will argue that it fits catadromy as well. They think that amphidromy is a life history strategy that allows these small bodied fishes to boost their fecundity relative to non-migratory conspecifics by producing tiny pelagic larvae, and consequently, this is a life history that is restricted to species that can rapidly transport their eggs or larvae into the sea from the adult freshwater habitat. And dispersal ends up as a useful, but incedental biproduct of this strategy. But there’s a catch, and that is that when you produce lots of small eggs, it leaves limited resources for individual larvae which are then prone to starvation if they don’t make it into the ocean rapidly enough. Closs, Hicks & Jellyman (2013) Freshwater Biology

Amphidromy & Torrentfish Endemic New Zealand amphidromous fish Max length 150 mm, > 50,000 tiny eggs Penetrates up to ~220 km inland in low gradient but fast flowing rivers & streams How to get eggs/larvae to sea quickly? Evidence for migration Females upstream, males downstream Suggested females must migrate to spawn The species that I’m focusing on as part of my PhD research is the New Zealand torrentfish. It’s a fairly typical amphidromous fish in that it’s relatively small at 150mm but has very high fecundity, with ripe females holding between 30 and 50k eggs. It’s unusual in that it can occur up to 220km inland in lower gradient systems, and this poses the question. How is an obligate diadromous fish transporting its eggs 200km to the sea? Well there’s some evidence for migration in the species in the form of research showing that they’re sexually segregated, with the females living upstream and the males downstream, which would suggest that females must be migrating downstream to meet the males and spawn. Bruno David Scrimgeour & Eldon (1989) N Z J Mar Freshw Res

Aims Do torrentfish migrate downstream to spawn? Torrentfish size & sex distribution across multiple rivers at varying distances inland Monthly size / sex structure of torrentfish along Waianakarua River So the aim of my study was to determine whether torrentfish were migrating downstream to spawn, and I did this by looking at size and sex distributions across multiple rivers at varying distances inland, as well as monitoring demographics monthly along a single river.

Methods Electrofishing of 21 sites in 12 South Island river systems 20 fish retained per sampling, dissected & sexed Includes juveniles & adults Longtitudinal monthly monitoring on Waianakarua River at four sites Non-lethal sampling Mature ripe fish sexed based on external appearance My methods were fairly straightforward and we electrofished 21 sites in 12 rivers, keeping 20 fish per site, and we dissected these fish to determine their sex. At the monitoring site, we did catch and release monitoring, and sexed mature fish based on external characteristics.

Here’s an example of a ripe female torrentfish on the left and a male on the right, you could tell ripe males from females because they would express milt when handled. Manna Warburton

Multi-River Study – Sex/Size vs Inland Penetration Males Juvenile grow as migrate inland Progressive downstream migration at begins at maturity Largest males located near river mouth Prime spawning habitat? So here’s what we found for male torrentfish in the multi-river group. Juveniles invade at about 30-40mm total length and steadily move inland as they grow, till they reach about 70mm, which is about the time they become sexually mature.

Multi-River Study – Sex/Size vs Inland Penetration Males Juvenile grow as migrate inland Progressive downstream migration at begins at maturity Largest males located near river mouth Prime spawning habitat? At this point they start heading back downstream, and we find the largest adult males at sites closest to the ocean, which is likely to be where the majority of spawning is taking place

Multi-River Study – Sex/Size vs Inland Penetration Females Juveniles grow as migrate inland Mixed age / size downstream Females migrating downstream at different ages or up and downstream? Short period at spawning sites The pattern for females is the same for juvenile fish

Multi-River Study – Sex/Size vs Inland Penetration Females Juveniles grow as migrate inland Mixed age / size downstream Females migrating downstream at different ages or up and downstream? Short period at spawning sites They grow and invade inland up to about 70mm

Multi-River Study – Sex/Size vs Inland Penetration Females Juveniles grow as migrate inland Mixed age / size downstream Females migrating downstream at different ages or up and downstream? Short period at spawning sites At this point they may be returning downstream at different ages

Multi-River Study – Sex/Size vs Inland Penetration Females Juveniles grow as migrate inland Mixed age / size downstream Females migrating downstream at different ages or up and downstream? Short period at spawning sites Or going downstream and spawning before migrating back upstream and then down again to spawn again, but whatever they’re doing, they don’t seem to be hanging around downstream

Monthly Size / Sex Distribution Study Time (Julian Date) Size (mm) Upstream Downstream Waianakarua River So here’s the data from the monthly demographic monitoring, with each of these box plots representing a visit to these two sites, which were an upstream site that was mostly female, and a downstream site that was mostly male.

Monthly Size / Sex Distribution Study Time (Julian Date) Size (mm) Upstream Downstream Mostly ripe females Waianakarua River Mostly ripe males Ripe males & females What we saw was a cohort of large adult females become increasingly less common at this upper site, and become more common at the downstream site over the course of a single breeding season

Migration in Torrentfish Torrentfish are migrating to spawn Majority of spawning takes place in lower reaches Spawning in downstream locations reduces larval migration times Based on our sampling, we think that torrentfish are migrating to spawn, and that spawning is taking place in the lower reaches of the systems these fish occupy. And it’s our hypothesis that spawning in these downstream locations reduces both the distance and the time it takes for these very small larvae to reach the marine nursery habitat.

Downstream Migration in Amphidromous & Catadromous Fish Pattern of downstream migration to spawn not unique to torrentfish Common feature amongst amphidromous species that inhabit low gradient rivers A potential strategy to reduce distance of downstream larval transport to sea With near-catadromous & catadromous strategies being ‘extensions’ of this transport mechanism When we look at other examples of migration in amphidromous fishes, we find that this is actually a common feature of species that specifically inhabit low gradient systems. Like I said before, we think that this is a strategy to reduce the time and distance larvae have to travel to reach the sea, and from here it’s not much further to migrate into the estuary, or the nearshore marine environment, and into a fully catadromous life history.

Amphidromy, Catadromy & River Gradient Stream Gradient Headwaters to Sea Barrier Steep & fast discharge to sea Moderate inland penetration Amphidromous with no down-stream migration Transport relies entirely on larval drift Many Galaxias, Gobiidae, Cottidae Low gradient & fast discharge to sea Considerable inland penetration Amphidromous but with migration downstream Spawning in freshwater above estuary Torrentfish, Awaous guamensis, Australian grayling, Ayu Low gradient & slow discharge to sea Considerable inland penetration Near-catadromy or catadromy Downstream migration to estuary or sea overcome barrier to passive transport Galaxias maculatus, tupong, many others When we look across the landscape at patterns of species distribution, we find amphidromous fishes with no downstream migration occupying steep, high gradient systems that afford rapid transport of larvae into the sea, and we find these species only a moderate distance inland. As gradient decreases, we find amphidromous fishes that engage in downstream migrations, and these species can often penetrate long distances inland. Finally as systems become extremely low gradient, with tidally influenced lower reaches, we see near catadromous and fully catadromous life histories dominating.

Conclusion Propose that amphidromy & catadromy are functionally equivalent Enables high fecundity by production of tiny pelagic larvae But lowland barriers to larval transport increase as gradient & speed of discharge to sea declines Requires increasing levels of ‘parental assistance’ for rapid transfer of larvae Distribution of different strategies reflects response to coastal landscape & hydrology So in conclusion, if you accept Closs’s interpretation of amphidromy, and by extension catadromy, as life histories associated with increasing fecundity through the production of tiny pelagic larvae, then the two life histories can be viewed as a single functionally equivalent strategy, where barriers to larval transport associated with gradient and discharge are mediated by increasing levels of parental assistance for the rapid transfer of larvae into the marine environment, with the distribution of different strategies being a response to coastal landscapes and hydrology

Thanks to Environment Southland Department of Conservation University of Otago Closs Lab In closing I’d like to thank Environment Southland, the Department of Conservation, and the University of Otago, as well as my lab mates for their support in making this work possible