Field work ethics in biological research

Gulls_over_a_fishing_trawler_Ste_01

Costello et al. 2016. Field work ethics in biological research. Biological Conservation. 203:268-271.


Birdringingphoto

Eilidh McNab

This week’s journal club, whilst focussed on a single article, was also a chance for the group to have a wider discussion around the ethics of field work.

Historically much natural history research has been undertaken through ‘collecting’ specimens – i.e. killing and preserving individuals. The scientific descriptions of most species on the planet come from ‘type’ specimens held in museums; the individual(s) from which the species is defined and named. Early ornithologists went out birding with shotguns, not binoculars. However, in recent decades this view of biological science has been gradually replaced by non-lethal methods (such as camera-trapping, DNA analysis, radio-tracking, etc.) and the use of fatal collecting methods (certainly amongst vertebrates) is growing increasingly rare (aside from e.g. medical research, which I will not discuss here).

In this week’s paper, Costello et al. (all editors of the journal Biological Conservation, in which the paper is published) confront the ongoing issue of articles submitted to the journal that have, in their view, involved the unnecessary lethal collection of vertebrates, and have therefore been rejected for publication. The three recent examples that the authors discuss involved fish; in two instances researchers employed the use of gill-nets (which often lead to mortality of other non-target species as well), and in another there were very high rates of mortality due to tagging in a capture-release study. Importantly, in all instances the papers were not investigating a novel idea; instead they were simply showing well-understood phenomena in a different location. A table presenting a checklist of considerations for respectful conduct during field sampling highlights this as an important point; any negative impacts must be justifiable in terms of the advancement of scientific knowledge. However, as was pointed out in our debate on this paper, often it is not known what the results may be in advance of a study! Even fairly closely-related species can react very differently, and without first carrying out the field research this can’t necessarily be predicted.

Whilst lethal collecting or increased mortality due to methodology are the main topics, the paper discusses a number of other important issues surrounding field research. One of the first sections highlights the “uneven treatment of species”; and whether the relevant authorities (be they university ethics committees, or government officials) are more likely to allow lethal collection of one taxa over another. They ponder whether the case studies discussed involving fish would have been given permission had it been birds, mammals or reptiles involved – most likely not. This led to some discussion in the group about how much we understand about the way fish react to stimuli; a recent study looked at the use of compounds commonly used to euthanise laboratory zebrafish specimens, which was assumed to slowly send them to sleep. This compound was actually shown to drastically alter their behaviour prior to death, forcing the normally shade-seeking fish out into brightly lit areas of the tank. If this is the behavioural response, can we truly understand how the fish are reacting internally? And is it really as humane as was formerly thought?

Another important topic discussed within the paper was the impacts to non-target species that may result from any programme of fieldwork. This could include trampling (of vegetation or of e.g. invertebrates), or the transfer of invasive plant species or diseases (such as the fungus that causes white-nosed syndrome in North American bats, which has wiped out millions of individuals; the disease may have been inadvertently introduced by European-based cavers or bat ecologists).

The paper finished with a number of different solutions to the issues discussed. This included the use of low-impact methods where at all practicable, such as camera-traps, hair and faeces collection, drones, and observations. They also highlighted the importance of applying the ‘precautionary principle’ to research work, and to consider the possible impacts to the whole ecosystem being studied, not necessarily just the target species.

What is not really discussed in the paper is the perspective of different ‘types’ of researcher; for example a virologist may have a different view of lethal collecting to a conservation biologist. Another point that was brought up during our discussions, but is again not mentioned in the paper, is the cultural significance of certain organisms. Whilst a university ethics board may approve the lethal collection of a species, if it is viewed as particularly important, maybe even sacred, to native peoples in the study area, this should certainly be an important consideration for any researcher.

Whilst the paper is only three pages long, it succinctly covers a range of key considerations when planning any programme of field work. We concluded that this is an important paper to remind scientific researchers not just to fully explore all potential sampling methods before resorting to lethal collecting, but also to consider other potentially negative impacts that could be caused by the study. For example disturbance to other non-target organisms and the spreading of invasive species due to researcher movements should be considered prior to any research work. Whilst there were some comments that the paper may be viewed as a little ‘preaching to the converted’, the fact that multiple papers have been submitted to Biological Conservation that do not meet the ethical standards set by the journal highlights that it is still an important topic to discuss. This importance is highlighted by the fact that this article is one of the most downloaded from the journal in the last 90 days.

Join us this Friday when Matt Guy will lead a discussion on a recent paper in PloS ONE by Angell et al. entitled Sexual Segregation and Flexible Mating Patterns in Temperate Bats.

http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0054194

External morphology explains the success of biological invasions

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Azzurro et al. 2014 External morphology explains the success of biological invasions. Ecology Letters 17: 1455-1463.


zarah

Zarah Pattison

There is rarely a shortage of papers attempting to explain why particular species are more or less invasive than others. Since Charles Elton’s seminar work in 1958 (The Ecology of Invasions by Animals and Plants) there has been a rapid increase, particularly in the last 20 years, in publications surrounding the topic of invasion ecology. The silver bullet to help prevent invasions would be to determine which characteristics contribute most to invasion success and therefore enable us to predict the seriousness of an invasion for prevention and management. Azzuro et al. (2014) offered something a bit unique in their attempt to explain invasiveness by using the external morphology of species, fish species in this instance.

The aim of this study was to explore whether morphological traits could explain the abundance of introduced fish species entering the Mediterranean Sea via the Suez Canal. The Mediterranean Basin is suggested to have a monopoly of vacant niches, which may be contributing to the successful establishment of invasive species therein. Therefore the use of species morphology as a proxy for its ecological status in a community, could explain niche availability and the potential population increase post establishment.

Our initial thoughts were positive. The paper was written well, succinct and enjoyable. A large data set was used in an analysis which none of us had expertise in, but it was still clear what the authors were trying to achieve. (Very) basically a polygon encompassing the morphological space of the native fish community was used and the traits of non-native fish species were plotted across the native morphospace. The results showed that invasive non-native fish species were more abundant either outside or on the outer perimeter of the native morphospace where niche occupancy was low. Non-native species morphologically similar to native species, were less abundant and less likely to establish.

The paper definitely added to the breadth of our invasion ecology knowledge. However, like most studies in invasion ecology, the results are difficult to generalise. Negative caveats of many invasion ecology papers focused on specific species are just that: species specific and not amenable to generalisation. This can be frustrating from a conservation point of view. The authors themselves discussed the limitations of this study particularly in the case of invasive non-native lionfish (Pterois spp.) which has a rather unique morphology. Another point raised was that environmental conditions were not taken into account in this study, particularly fishing quotas which could lead to fluctuating populations regardless of native status. Additionally, life history/functional traits, which are used in many plant invasion studies, were not considered.

Overall the paper delivered its aim, but the title is very confident. Perhaps “External morphology can additionally explain the success of species specific biological invasions” would be more appropriate. However, we can’t test for everything in a study (we all know this!) and we all agreed this was a good piece of interesting science.

Join us next week where Eilidh McNab will lead a discussion of a paper recently published in Biological Conservation entitled: Field work ethics in biological research.

Hyperdominance in the Amazonian tree flora

Hyperdominance in the Amazonian Tree Flora. ter Steeg et al. Science 342 (6156). DOI:10.1126/science.1243092. Hyperdominance in the Amazonian tree flora

I can't see the Amazon for all these tree plots - taken from ter Steege et al.

I can’t see the Amazon for all these tree plots – taken from ter Steege et al.


Jun Lim

Jun Lim

Among other things, the authors set out to try to estimate how many tree species are in the Amazon, how they are distributed in space and among habitat types. They did this in part by extrapolating the total Amazonian tree diversity by fitting the mean rank-abundance data for over half a million trees within 1,000 well-studied plots in the Amazon to Fisher’s log-series. They found that there were “hyper-dominant” tree species, which represented about 1.4% of Amazonian tree diversity while representing over half of all trees in the Amazon. On the other hand, the rarest 11,000 species accounted for a paltry 0.1% of all trees! Furthermore, as it turns out, this inequity in abundance among tree species in the Amazon had an interesting spatial pattern. These so-called “hyper-dominants”, had on average larger geographic ranges, but the majority of them were found to be dominant in only one or two out of several distinct forest types, suggesting that dominant species were habitat-specialists.

This paper, however, leaves me with an intense wanting, although these findings are clearly the first of many awesome papers to come. Firstly, it would be interesting to see how these patterns of dominance generalize to other tropical tree systems, such as the ever-wet forests of South-east Asia (where I grew up, albeit in the virtually deforested Singapore). Anybody who knows even a little of the rainforests of Malaysia and Indonesia thinks immediately of the dipterocarp trees (Dipterocarpaceae) that form much if not most of the canopy.

Another thing that really got me thinking was the idea of scalar-dependency in niche specialism. Sure, if you are a species that does well in one particular soil type, all the small-scale heterogeneity in habitat does not matter much to your distribution (kinda like generalism). But in the larger scheme of things, you start to appear much more constrained (specialism). What’s interesting is that this plays out in a consistent and similar way across many species and across many different habitats. From a community assembly standpoint, this brings up the age old question of the relative importance of dispersal limitation (high numbers of species can effectively coexist even if a habitat was homogeneous) and niche-based explanations for high species diversity, especially considering the strong role of habitat heterogeneity across many systems (which filters for different communities in different parts of the landscape). I feel it is still unlikely that the relative role of these two processes will be disentangled any time soon, although this paper was a big step towards that goal.


Will Pearse

Will Pearse

It’s hard to think of an image in ecology that represents much more blood, sweat, and tears than the one at the top of this article. 567 plots would be a lot anywhere in the world, but dense Amazonian rainforest does not make for easy fieldwork. That you can go online, register, and download much of this data right now makes this even more wonderful; thank you everyone involved in RAINFOR!

Like Jun, I sense this is the first of many papers working with this dataset (and is an excellent start at that!), but I sense it may still take us some time yet to get a handle on the Amazon! I’m having some trouble getting my head around the spatial scale of this dataset, and so I’m unsure how I feel about the most common (hyperdominant) species in the Amazon being habitat specialists. In many ways I’d be shocked if species were truly generalists in the sense that they were everywhere across the Amazon, although I suppose I’d need a dataset like this to be sure! I’m particularly interested by how more diverse genera are less likely to contain hyperdominants. I’m tempted to infer that because hyper-diverse genera are more similar to one-another and have similar ranges, they are competing too strongly with one-another to become dominant. Given there’s a taxonomic effect to hyperdominance, perhaps a phylogenetic analysis would help get at these issues (…although I’d rather not be the one making a phylogeny of the Amazon…!)

I think it’s legitimate to ask how many species there are in the Amazon using this dataset, and I’m frankly amazed by how flat the middle of the rank-abundance plot in figure 2 is for the Amazon. While I agree with the authors’ general conclusions here, I am slightly concerned about extrapolating out into such low population sizes. It’s probably fair to say that no one single curve can describe both the hyperdominant and extremely rare species in the Amazon, and the extrapolation is based on assuming that a straight line that follows the medium-richness species will cover everything. I’m sure the authors would agree that this is a simplification; naively I would expect expect this estimate to be too high, yet their estimate of ~15000 species in the Amazon actually struck me as quite low when I first saw it. I guess much of this might fall back to what we’d be happy considering a species; trees are not known for playing by phylogeneticists’ rules, and maybe very rare species can survive for quite a while in the Amazon thanks to outcrossing and hybridisation.


Lynsey McInnes

Lynsey McInnes

I always open a Science paper with a slight sense of foreboding that if I want to understand even a little of what the authors have done, I’ll have to trawl through endless supplementary files. So, first things first, I really appreciate the slightly longer format of this article so that by the end of it, you have a sense of what was done, alongside the pitfalls and the potential implications. A real, whole paper; result!

And what a paper. My mind is still a bit fluffy on the spatial scale and connectedness of each plot (I was surprised there was no map figure of the interpolated richness per 1 degree cell), but that is a minor grumble. This is a massive, impressive collaborative effort to probe the distribution of trees in Amazonia. Naively, I was taken aback by a number of findings: that there are potentially >16,000 tree species (seems like a lot to me), that only 227 of them seem to dominant, that each hyper-dominant was kinda habitat-restricted. Conversely, I wasn’t surprised that species in different families were distributed differently (one or a few hyper-dominants vs. tons of restricted-range endemics) or that two well-chosen traits didn’t predict hyper-dominance.

It’s clear that such a big effort is going to generate tons of follow-on papers, many of which have been primed in this first article. There seemed to be some confusion whether to focus on the hyper-dominants and what made them so vs. the thousands of species with tiny or unknown distributions many of which the authors suggest are close to extinction. An interesting route by which the authors will follow up this paper will likely be to try to find out how important the non-dominant species are for ecosystem functioning. They seem to suggest that perhaps they are not so important. I wonder what the cut-off for usefulness vs. exciting rarity is? Does it vary among plant families? How much could we lose without having any impact at all? How much complementarity is there? How easy (and valid) will be to model ecosystem functioning or resource cycling concentrating only or mostly on the hyper-dominants?

I also found it funny that the authors did not wonder why their Maxent models predicted populations of many species in places where extensive surveys suggest they are not found. What is found in their place? Populations of phylogenetically or functionally related species? Or was some environmental or topographic variable missing? An easy (but perhaps quite dull) follow-on paper perhaps…

A final follow-on that I could think of would be to compare spatial patterns of some of the species’ patterns (a mix of hyper and non-hyper dominants) among regions and forest types (kinda like figure 4) to see if one can tease out any patterns of dispersal limitation. I think the authors conclude that many species are restricted to one or two forest types: are these generally within a region or across all or multiple regions (this might have been covered, but I missed it). If you are happy with the high levels of extrapolation (interpolation?) involved, this dataset is a treasure chest for dispersal ecologists…

So many options! And more or less freely-available online already (see link above). Let’s get going!

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