Functional extinction of birds drives rapid evolutionary changes in seed size

Galetti et al. Science 340(6136): 1086-1090. DOI:0.1126/science.1233774. Functional extinction of birds drives rapid evolutionary changes in seed size

Birds only disperse what they can carry! From Galetti et al.

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Will Pearse

Wam-bam, this is a paper I would have loved to put in my undergrad essays. Plants need birds to disperse their seeds, and so when large birds go locally-extinct, plants evolve smaller seeds that smaller birds can carry. This happens really, really fast (within the last 75/100 years!) and so is a great example of rapid evolution.

A nastier man than I would point out that this is somewhat inferred; with no data on what seed size was like 100 years ago there’s a fair bit of supposition going on here. However, their variance decomposition (34% due to birds in forest, 0.1% differences among sites) is really quite striking, so I’m quite happy to go along with this. There’s such a clear link between seed size and probability of being dispersed (figure 2b) that I’m quite happy to accept the smoking gun of a huge selective pressure and observable differences.

Which leaves me with a slight problem, because I always assume that we can ignore both intraspecific variation and rapid evolution when doing ecosystem service work. If trait can evolve this rapidly, treating species’ ecosystem services and traits as fixed is no longer acceptable. Indeed, the situation is doubly problematic because there are going to be a lot of downstream effects of changing seed size, not just on the plant species itself (it’s now shifted on the simplified on the r vs. k selection spectrum), but also other species that interact with that plant. There is a huge literature on how phenology shifts are worse in tri-trophic interaction networks because not every component of the system can keep up with change – I see no reason for this not to be a concern here.

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Lynsey McInnes

This is to all intents and purposes a very neat demonstration of purported rapid evolutionary change in the face of a new selective pressure brough about by human-mediated loss of large-gaped frugivores from forest fragments. One could quibble on whether the frugivore loss is driving the contraction in seed size variation, or whether fragmentation caused the frugivore loss, and so on, but the authors do a thorough job of dismissing other possible correlates….environmental differences among sites, checking the time needed for such a response, and I’m pretty convinced the relationship holds.

This is bad news! It suggests many of those stacks of papers predicting responses to climate change or habitat fragmentation that brush evolutionary responses under the carpet are probably missing key elements of the response game, Similarly, how does this two trophic level result cascade to additional trophic levels. Without big palm seeds and thus big healthy palms, what grows in their place? What effect do these newly dominant plant species have on other pieces of the forest ecosystem.  Ah, its frightening.

What is the next step? Can we rejoin the forest fragments and get the large-gaped frugivores back? Is there enough genetic variation left to get back the large seeds?

This must have been a time-consuming study and its just not feasible to initiate tons of new studies at similar scales to ascertain how pervasive such rapid evolutionary responses are. I would naively guess that it might be better to continue with this system and see if we can work out this change’s effect on additional chunks of the forest ecosystem. Perhaps the authors are already working in that.

The macroecologist in me also ponders the feasibility and merits of expanding the scope of such studies. Perhaps to a mesoscale at least. I am reminded of Phillimore et al‘s very slick mesoscale studies on variation in phenological responses across space in British frogs. Here, the authors were looking to distinguish local adaptation vs. plasticity governing the spatial variation that they saw in order to predict how populations would cope in the face of climate change that will alter the timing of temperature cues. In short, the authors conclude climate change is expected to outpace the frogs’ ability to respond. However, they ignored the potential for microevolutionary change, as the timescales they were thinking of were so short. The challenge now seems to be to incorporate this possible response? Admittedly, easier said than done…

Unraveling the drivers of community dissimilarity and species extinction in fragmented landscapes

Banks-Leite et al. 2013. Ecology 93(12) 2560-2569. DOI:10.1890/11-2054.1. Unraveling the drivers of community dissimilarity and species extinction in fragmented landscapes

Below, we give our first impressions of this article. Please comment below, or tweet Will or Lynsey (maybe use #pegejc). Think of this as a journal club discussion group!

We both wrote our responses quite rapidly this week, but decided to post them anyway and hopefully start a discussion with our readers. Both of us found this paper thought-provoking and hope to have more coherent thoughts to add later in the week…

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Will Pearse

I picked this paper almost entirely on the basis of figure 1b – the fit looked so good I had to read the paper to find out what it meant. The central claim of this paper is that SAR curves miss changes in species composition when fragmentation takes place, meaning there is a disconnect between species richness and the local extinction of species. The quality of the analysis and the size of the dataset make this a particularly pleasant paper to read, and it reminded me of things (like SLOSS, see below) I haven’t thought about for some time.

The 1970s were a good time to be a conservation biologist: you could still fly to conferences without feeling too bad, and debate was raging about whether to have a Single Large Or Several Small (SLOSS) conservation reserve. This paper is a perfect example of why this debate was never fully resolved: larger fragments may have a higher species richness, but they don’t necessarily contain the same species as smaller fragments. To my mind, this is the clearest demonstration of this effect to date; figure 3d shows more species in larger fragments, but (crucially) there are species present in larger fragments that are absent from smaller fragments, and vice-versa. Going further, a fragment’s surroundings matter too: small fragments in pristine forest resemble larger fragments in near-pristine forest, but are nothing like the smaller fragments in heavily deforested surroundings. Hence all of the figures in this paper are sorted by surrounding forest cover, and then fragment size. Let me say this again: I don’t think I’ve ever seen such neat graphs. Ever.

Which is perhaps something to do with individuals’ range size. I’m no field biologist, but some birds fly quite a long way during the day, and others don’t. This means that different spatial scales of habitat damage are going to be relevant for different birds, and extreme logging of forests might be expected to affect wide-ranging birds first irrespective of the size of individual fragments. Could these kinds of traits, which reflect the use of the surroundings (matrix) by birds, be incorporated into further analyses? Perhaps similar things could be found when comparing among taxa – would insects that disperse only a few meters in their entire lifespan produce as nice graphs as these?

According to the supplementary materials, these fragments are ~40-60 years old, so (in my opinion) these are fairly mature fragments – we’re certainly not seeing the immediate after-effects of fragmentation. Which makes me wonder what those species that specialise in smaller habitat patches represent – what kind of Amazonian species is pre-adapted to small fragments of forest in a sea of deforestation? If they’re not that well-adapted to Amazonian living, and have only come in with deforestation, are they definitely using the forest fragments, and not just passing through? Is it possible to quantify the extent to which particular birds are using a resource? I’ll end on that – if anyone knows how this can be done with mist net data, please let me know. I’ve only done a tiny bit of mist-netting and pit-fall trapping in my time (I was dreadful!) and I often wonder how we’re meant to handle transient passers-by.

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Lynsey McInnes

Typically, I shrike at reading ‘Ecology’ papers – I’m not an ecologist I say to myself. Since joining a department more or less full with population geneticists, it turns out I AM an ecologist, albeit somewhat by accident. Needless to state, Will picked this paper and I went along with it because I like species-area relationships…

That was the first concept to be knocked down, turns out SARs suck at characterising community responses to habitat fragmentation! Ooops.

I found this paper really neat. Very cool, very precise question, amazing data, very sexy, very understandable simulations! I really have to stop myself going to have a play with the R code that does the simulations (also neat that this is provided!).

The rationale for the study and the conclusions they come up with seem robust to me, I am just now wondering whether there are any comparably good datasets where these questions could be asked again? Is such a comprehensive dataset necessary? (Probably yes, right?)

I’ve been a bit lazy and not read the J Appl Ecol. paper where the authors test a bunch of metrics to come up with an adequate one for community composition so I was a bit disappointed that the rationale/robustness/power of the measure chosen wasn’t better explained here. Is it biased in anyway? Does it miss anything?

With my macro-hat on, I wonder if this setup could be used to look at turnover/composition on broader temporal and spatial scales. For example, debate is still raging on ecological limits to diversity, lots of signals point to the diversity-dependence of cladogenesis and this is typically explained by niche filling (diversification slows down as niches get filled), lineages competing for limited resources/niche space. However, how does this really work on broad spatial scales where few lineages within a radiation will actually ever come into physical contact, let alone interact. And perhaps more relevant here, the region in which they diversify is not just one homogeneous blob, but a matrix of different sized habitable units more or less connected to each other. I’m rambling a little, but I think incorporating landscape features in models of spatially-explicit diversification may help in explaining the patterns that we see (I have to think more about this though).

Two more things:

1. I guess (and Will’s the expert here), on broader scales similar studies have been undertaken under the umbrella of community phylogenetics. I’m still getting a handle on how this study fits with the latter…Also, what would happen if we added a phylogenetic take on compositional turnover? Would it simplify things? Box out traits relevant to persistence in the different fragments?
2. What does this mean in terms of practical conservation guidelines now that we cannot fall back on the faithful SAR? It sounds to me like we need to get our hands on way more elaborate datasets of species identity and move from there into the traits that the different species bring to the fragments they can persist in. This sounds difficult. Are there any easy work-arounds?

Apologies for a very rambley, not well-thought out response to this article. In short, I really enjoyed it, it made me quite fearful for all those conservation decisions based on species numbers and made me thoughtful on whether these insights and setup could bring clarity to questions typically asked at different scales. Watch this space…