Authors: Evatt Chirgwin, Dustin J Marshall, and Keyne Monro
Published in:Functional Ecology
Abstract
Global warming may threaten fertility, which is a key component of individual fitness and vital for population persistence. For males, fertility relies on the ability of sperm to collide and fuse with eggs; consequently, sperm morphology is predicted to be a prime target of selection owing to its effects on male function.
In aquatic environments, warming will expose gametes of external fertilizers to the physiological effects of higher temperature and the physical effects of lower viscosity. However, the consequences of either effect for fertility, and for selection acting on sperm traits to maintain fertility, are poorly understood.
Here, we test how independent changes in water temperature and viscosity alter male fertility and selection on sperm morphology in an externally fertilizing marine tubeworm. To create five fertilization environments, we manipulate temperature to reflect current-day conditions (16.5 °C), projected near-term warming (21 °C) and projected long-term warming (25 °C), then adjust two more environments at 21 °C and 25 °C to the viscosity of environments at 16.5 °C and 21 °C, respectively. We then use a split-ejaculate design to measure the fertility of focal males, and selection on their sperm, in each environment.
Projected changes in temperature and viscosity act independently to reduce male fertility, but act jointly to alter selection on sperm morphology. Specifically, environments resulting from projected warming alter selection on the sperm midpiece in ways that suggest shifts in the energetic challenges of functioning under stressful conditions. Selection also targets sperm head dimensions and tail length, irrespective of environment.
We provide the first evidence that projected changes in ocean temperature and viscosity will not only impact the fertility of marine external fertilizers, but expose their gametes to novel selection pressures that may drive them to adapt in response if gamete phenotypes are sufficiently heritable.
Chirgwin E, Marshall DJ, Monro K (2019) Physical and physiological impacts of ocean warming alter phenotypic selection on sperm morphology. Functional EcologyPDFDOI
Authors: Hayley Cameron, Tim Coulson, and Dustin J Marshall
Published in:Ecology Letters
Abstract
Species simultaneously compete with and facilitate one another. Size can mediate transitions along this competition–facilitation continuum, but the consequences for demography are unclear.
We orthogonally manipulated the size of a focal species, and the size and density of a heterospecific neighbour, in the field using a model marine system. We then parameterised a size‐structured population model with our experimental data.
We found that heterospecific size and density interactively altered the population dynamics of the focal species. Size determined whether heterospecifics facilitated (when small) or competed with (when large) the focal species, while density strengthened these interactions.
Such size‐mediated interactions also altered the pace of the focal’s life history. We provide the first demonstration that size and density mediate competition and facilitation from a population dynamical perspective. We suspect such effects are ubiquitous, but currently underappreciated.
We reiterate classic cautions against inferences about competitive hierarchies made in the absence of size‐specific data.
Cameron H, Coulson T, Marshall DJ (2019) Size and density mediate transitions between competition and facilitation. Ecology LettersPDFDOI
Certain pathogens (disease-producing organisms) are stuck in a Catch-22; to survive they need to continue to find, and infect, new hosts. But infection makes their hosts sick and less likely to move to where there are new hosts to infect.
PhD student Louise Nørgaard and her supervisors Ben Phillips and Matt Hall have found evidence of a pathogen that resolves this issue by exploiting the differences in size and behaviour of male and female hosts to optimize its own chance of successful infection.
The team uses the freshwater crustacean Daphnia magna and its common pathogen Pasteuria ramosa as a model system to test the idea that a pathogen can exploit differences between the sexes of a host to its advantage. The pathogen P. ramosa is ingested by Daphnia after which it sterilises and kills the host, releasing transmission spores that are ready to infect a new host. Female Daphnia are bigger, live longer and are more susceptible to infection than males.
Louise set up two separate experiments, allowing her to monitor the probability that Daphnia would disperse from a crowded area to a less crowded area and to measure the rate and distance travelled by infected and uninfected male and female individuals.
In the first experiment Louise was able to capitalise on previous work that has shown that Daphnia will disperse when conditions are crowded. Exposure to water taken from high densities of Daphniais enough to encourage dispersal. Louise used ‘crowded-conditioned’ water and found infected male Daphnia were more likely to disperse than uninfected males. Infected females, on the other hand, were a lot less likely to disperse than uninfected females.
A second experiment found that infected females had four times the number of transmission spores than infected males and moved less far and more slowly than males or uninfected females. Infected males though, moved at the same rate and travelled the same distance as uninfected males.
The figure A shows how far male (blue) and females (green) disperse when infected with the pathogen compared to uninfected individuals. Louise tested two types of pathogen C1 and C19. She also measured the distance travelled (B) and the spore load in infected individuals (C).
So how do these differences between the sexes help the pathogen? Females are bigger and can host large numbers of transmission spores. Staying put when densities are high means they are releasing this large number of spores into a crowd – potentially maximising the chance of further infections. Smaller males have fewer spores to release and the chance of secondary infections may be maximised when they move to new areas where few individuals are already infected.
Importantly the differences in dispersal behaviour between infected males and females seem to relate directly to the way the pathogen interacts with each sex. Uninfected males and females had similar rates and distance of dispersal while uninfected females were more likely to move away from crowded habitats than males. These patterns disappear when both sexes are infected.
Do these different infection strategies in different sexes provide a form of bet-hedging for the pathogen? Louise and her supervisors think they do and, if widespread, will have important implications for disease dynamics.
Offspring sizes vary within populations but the reasons are unclear. Game‐theoretic models predict that selection will maintain offspring‐size variation when large offspring are superior competitors (i.e., competition is asymmetric), but small offspring are superior colonizers. Empirical tests are equivocal, however, and typically rely on interspecific comparisons, whereas explicit intraspecific tests are rare.
In a field study, we test whether offspring size affects competitive asymmetries using the sessile marine invertebrate, Bugula neritina. Surprisingly, we show that offspring size determines whether interactions are competitive or facilitative — large neighbours strongly facilitated small offspring, but also strongly competed with large offspring. These findings contradict the assumptions of classic theory — that is, large offspring were not superior competitors. Instead, smaller offspring actually benefit from interactions with large offspring— suggesting that asymmetric facilitation, rather than asymmetric competition, operates in our system.
We argue that facilitation of small offspring may be more widespread than currently appreciated, and may maintain variation in offspring size via negative frequency‐dependent selection.
Offspring size theory has classically viewed offspring interactions through the lens of competition alone, yet our results and those of others suggest that theory should accommodate positive interactions in explorations of offspring‐size variation.
Cameron H, Marshall DJ (2019) Can competitive asymmetries maintain offspring size variation? A manipulative field test. Evolution PDFDOI
About half of the coastline of Europe, the United States and Australasia is modified by artificial structures. In newly published research, we identified a new effect of marine urbanisation that has so far gone unrecognised.
When we build marinas, ports, jetties and coastal defences, we introduce hard structures that weren’t there before and which reduce the amount of sunlight hitting the water. This means energy producers such as seaweed and algae, which use light energy to transform carbon dioxide into sugars, are replaced by energy consumers such as filter-feeding invertebrates. These latter species are often not native to the area, and can profoundly alter marine habitats by displacing local species, reducing biodiversity, and decreasing the overall productivity of ecosystems.
Incorporating simple designs in our marine infrastructure to allow more light penetration, improve water flow, and maintain water quality, will go a long way towards curbing these negative consequences.
Pier life
We are used to thinking about the effects of urbanisation in our cities – but it is time to pay more attention to urban sprawl in the sea. We need to better understand the effects on the food web in a local context.
Most animals that establish themselves on these shaded hard structures are “sessile” invertebrates, which can’t move around. They come in a variety of forms, from encrusting species such as barnacles, to tree-shaped or vase-like forms such as bryozoans or sponges. But what they all have in common is that they can filter out algae from the water.
In Australian waters, we commonly see animals from a range of different groups including sea squirts, sponges, bryozoans, mussels and worms. They can grow in dense communities and often reproduce and grow quickly in new environments.
The sheltered and shaded nature of marine urbanisation disproportionately favours the development of dense invertebrate communities, as shown here in Port Phillip Bay.
How much energy do they use?
In our new research, published in the journal Frontiers in Ecology and the Environment, we analysed the total energy usage of invertebrate communities on artificial structures in two Australian bays: Moreton Bay, Queensland, and Port Phillip Bay, Victoria. We did so by combining data from field surveys, laboratory studies, and satellite data.
We also compiled data from other studies and assessed how much algae is required to support the energy demands of the filter-feeding species in commercial ports worldwide.
In Port Phillip Bay, 0.003% of the total area is taken up by artificial structures. While this doesn’t sound like much, it is equivalent to almost 50 soccer fields of human-built structures.
We found that the invertebrate community living on a single square metre of artificial structure consumes the algal biomass produced by 16 square metres of ocean. Hence, the total invertebrate community living on these structures in the bay consumes the algal biomass produced by 800 football pitches of ocean!
Similarly, Moreton Bay has 0.005% of its total area occupied by artificial structures, but each square metre of artificial structure requires around 5 square metres of algal production – a total of 115 football pitches. Our models account for various biological and physical variables such as temperature, light, and species composition, all of which contribute to generate differences among regions.
Overall, the invertebrates growing on artificial structures in these two Australian bays weigh as much as 3,200 three-tonne African elephants. This biomass would not exist were it not for marine urbanisation.
Colonies of mussels and polychaetes near Melbourne.
How does Australia compare to the rest of the world?
We found stark differences among ports in different parts of the world. For example, one square metre of artificial structure in cold, highly productive regions (such as St Petersburg, Russia) can require as little as 0.9 square metres of sea surface area to provide enough algal food to sustain the invertebrate populations. Cold regions can require less area because they are often richer in nutrients and better mixed than warmer waters.
In contrast, a square metre of structure in the nutrient-poor tropical waters of Hawaii can deplete all the algae produced in the surrounding 120 square metres.
All major commercial ports worldwide with associated area of the underwater artificial structures (size of grey dots) and trophic footprint (size of red borders). Trophic footprints indicate how much ocean surface is required to supply the energy demand of the sessile invertebrate community growing on all artificial structures of the port, averaged over the year. This depends on local conditions of ocean primary productivity and temperature. Ports located in cold, nutrient-rich waters (dark blue) have a lower footprint than ports in warmer waters (light blue).
Does it matter?
Should we be worried about all of this? To some extent, it depends on context.
These dense filter-feeding communities are removing algae that normally enters food webs and supports coastal fisheries. As human populations in coastal areas continue to increase, so will demand on these fisheries, which are already under pressure from climate change. These effects will be greatest in warmer, nutrient-poor waters.
But there is a flip side. Ports and urban coastlines are often polluted with increased nutrient inputs, such as sewage effluents or agricultural fertilisers. The dense populations of filter-feeders on the structures near these areas may help prevent this nutrient runoff from triggering problematic algal blooms, which can cause fish kills and impact human health. But we still need to know what types of algae these filter-feeding communities are predominantly consuming.
Our analysis provides an important first step in understanding how these communities might affect coastal production and food webs.
In places like Southeast Asia, marine managers should consider how artificial structures might affect essential coastal fisheries. Meanwhile, in places like Port Phillip Bay, we need to know whether and how these communities might affect the chances of harmful algal blooms.
One hectare of ocean in which fishing is not allowed (a marine protected area) produces at least five times the amount of fish as an equivalent unprotected hectare, according to new research published today.
This outsized effect means marine protected areas, or MPAs, are more valuable than we previously thought for conservation and increasing fishing catches in nearby areas.
Previous research has found the number of offspring from a fish increases exponentially as they grow larger, a disparity that had not been taken into account in earlier modelling of fish populations. By revising this basic assumption, the true value of MPAs is clearer.
Marine Protected Areas
Marine protected areas are ocean areas where human activity is restricted and at their best are “no take” zones, where removing animals and plants is banned. Fish populations within these areas can grow with limited human interference and potentially “spill-over” to replenish fished populations outside.
Obviously MPAs are designed to protect ecological communities, but scientists have long hoped they can play another role: contributing to the replenishment and maintenance of species that are targeted by fisheries.
Wild fisheries globally are under intense pressure and the size fish catches have levelled off or declined despite an ever-increasing fishing effort.
Yet fishers remain sceptical that any spillover will offset the loss of fishing grounds, and the role of MPAs in fisheries remains contentious. A key issue is the number of offspring that fish inside MPAs produce. If their fecundity is similar to that of fish outside the MPA, then obviously there will be no benefit and only costs to fishers.
Big fish have far more babies
Traditional models assume that fish reproductive output is proportional to mass, that is, doubling the mass of a fish doubles its reproductive output. Thus, the size of fish within a population is assumed to be less important than the total biomass when calculating population growth.
But a paper recently published in Science demonstrated this assumption is incorrect for 95% of fish species: larger fish actually have disproportionately higher reproductive outputs. That means doubling a fish’s mass more than doubles its reproductive output.
When we feed this newly revised assumption into models of fish reproduction, predictions about the value of MPAs change dramatically.
Fish are, on average, 25% longer inside protected areas than outside. This doesn’t sound like much, but it translates into a big difference in reproductive output – an MPA fish produces almost 3 times more offspring on average. This, coupled with higher fish populations because of the no-take rule means MPAs produce between 5 and 200 times (depending on the species) more offspring per unit area than unprotected areas.
Put another way, one hectare of MPA is worth at least 5 hectares of unprotected area in terms of the number of offspring produced.
We have to remember though, just because MPAs produce disproportionately more offspring it doesn’t necessarily mean they enhance fisheries yields.
For protected areas to increase catch sizes, offspring need to move to fished areas. To calculate fisheries yields, we need to model – among other things – larval dispersal between protected and unprotected areas. This information is only available for a few species.
We explored the consequences of disproportionate reproduction for fisheries yields with and without MPAs for one iconic fish, the coral trout on the Great Barrier Reef. This is one of the few species for which we had data for most of the key parameters, including decent estimates of larval dispersal and how connected different populations are.
We found MPAs do in fact enhance yields to fisheries when disproportionate reproduction is included in relatively realistic models of fish populations. For the coral trout, we saw a roughly 12% increase in tonnes of caught fish.
There are two lessons here. First, a fivefold increase in the production of eggs inside MPAs results in only modest increases in yield. This is because limited dispersal and higher death rates in the protected areas dampen the benefits.
However the exciting second lesson is these results suggest MPAs are not in conflict with the interests of fishers, as is often argued.
While MPAs restrict access to an entire population of fish, fishers still benefit from from their disproportionate affect on fish numbers. MPAs are a rare win-win strategy.
It’s unclear whether our results will hold for all species. What’s more, these effects rely on strict no-take rules being well-enforced, otherwise the essential differences in the sizes of fish will never be established.
We think that the value of MPAs as a fisheries management tool has been systematically underestimated. Including disproportionate reproduction in our assessments of MPAs should correct this view and partly resolve the debate about their value. Well-designed networks of MPAs could increase much-needed yields from wild-caught fish.
Authors: Martino E Malerba, Craig R White, and Dustin J Marshall
Published in: Frontiers in Ecology and the Environment
Abstract
Artificial structures are proliferating along coastlines worldwide, creating new habitat for heterotrophic filter feeders. The energy demand of this heterotrophic biomass is likely to be substantial, but is largely unquantified.
Combining in situ surveys, laboratory assays, and information obtained from geographic information systems, we estimated the energy demands of sessile invertebrates found on marine artificial structures worldwide.
At least 950,000 metric tons of heterotrophic biomass are associated with commercial ports around the world, emitting over 600 metric tons of carbon dioxide into the atmosphere and consuming 5 million megajoules of energy per day.
We propose the concept of a trophic “footprint” of marine urbanization, in which every square meter of artificial structure can negate the primary production of up to 130 square meters of surrounding coastal waters; collectively, these structures not only act as energy sinks and carbon sources, but also potentially reduce the productivity of coastal food webs.
Malerba ME, White CR, Marshall DJ (2019) The outsized trophic footprint of marine urbanization. Frontiers in Ecology and the EnvironmentPDFDOI
Authors: Dustin J Marshall, Steven Gaines, Robert Warner, Diego R Barneche, and Michael Bode
Published in: Frontiers in Ecology and the Environment
Abstract
Marine protected areas (MPAs) are important tools for managing marine ecosystems. MPAs are expected to replenish nearby exploited populations through the natural dispersal of young, but the models that make these predictions rely on assumptions that have recently been demonstrated to be incorrect for most species of fish.
A meta‐analysis showed that fish reproductive output scales “hyperallometrically” with fish mass, such that larger fish produce more offspring per unit body mass than smaller fish. Because fish are often larger inside MPAs, they should exhibit disproportionately higher reproductive output as compared to fish outside of MPAs.
We explore the consequences of hyperallometric reproduction for a range of species for population replenishment and the productivity of exploited species.
We show that the reproductive contribution of fish inside MPAs has been systematically underestimated and that fisheries yields can be enhanced by the establishment of reservoirs of larger, highly fecund fish.
Marshall DJ, Gaines S, Warner R, Barneche DR, Bode M (2019) Underestimating the benefits of marine protected areas for the replenishment of fished populations. Frontiers in Ecology and the EnvironmentPDFDOI
Authors: Louise Solveig Nørgaard, Ben L Phillips, and Matthew D Hall
Published in:Biology Letters
Abstract
Pathogens often rely on their host for dispersal. Yet, maximizing fitness via replication can cause damage to the host and an associated reduction in host movement, incurring a trade-off between transmission and dispersal.
Here, we test the idea that pathogens might mitigate this trade-off between reproductive fitness and dispersal by taking advantage of sexual dimorphism in their host, tailoring responses separately to males and females.
Using experimental populations of Daphnia magna and its bacterial pathogen Pasteuria ramosa as a test-case, we find evidence that this pathogen can use male hosts as a dispersal vector, and the larger females as high-quality resource patches for optimized production of transmission spores.
As sexual dimorphism in dispersal and body size is widespread across the animal kingdom, this differential exploitation of the sexes by a pathogen might be an unappreciated phenomenon, possibly evolved in various systems.
Nørgaard LS, Phillips BL, Hall MD (2019) Can pathogens optimize both transmission and dispersal by exploiting sexual dimorphism in their hosts? Biology LettersPDFDOI
Body size often strongly covaries with demography across species. Metabolism has long been invoked as the driver of these patterns, but tests of causal links between size, metabolism and demography within a species are exceedingly rare.
We used 400 generations of artificial selection to evolve a 2,427% size difference in the microalga Dunaliella tertiolecta. We repeatedly measured size, energy fluxes and demography across the evolved lineages. Then, we used standard metabolic theory to generate predictions of how size and demography should covary based on the scaling of energy fluxes that we measured.
The size dependency of energy remained relatively consistent in time, but metabolic theory failed to predict demographic rates, which varied unpredictably in strength and even sign across generations.
Classic theory holds that size affects demography via metabolism – our results suggest that both metabolism and size act separately to drive demography and that among‐species patterns may not predict within‐species processes.
Malerba ME, Marshall DJ (2019) Size-abundance rules? Evolution changes scaling relationships between size, metabolism and demography. Ecology Letters PDFDOI
Centre for Geometric Biology 