One of the long-standing questions in evolutionary ecology is on the mechanisms involved in arms race coevolution. One way to address this question is to understand the conditions under which one species evolves traits in response to the presence of a second species and so on. However, specialized pairwise interactions are by far less common in nature than interactions involving a higher number of interacting species (Bascompte, Jordano 2013). While interactions between large sets of species are the norm rather than the exception in mutualistic (pollination, seed dispersal), and antagonist (herbivory, parasitism) relationships, few is known on the way species identify, process, and respond to information provided by other interacting species under field conditions (Schaefer, Ruxton 2011). 

Zu et al. (2020) addressed this general question by developing an interesting information theory-based approach that hypothesized conditional entropy in chemical communication plays a role as proxy of fitness in plant-herbivore communities. More specifically, plant fitness was assumed to be related to the efficiency to code signals by plant species, and herbivore fitness to the capacity to decode plant signals. In this way, from the plant perspective, the elaboration of plant signals that elude decoding by herbivores is expected to be favored, as herbivores are expected to attack plants with simple chemical signals. The empirical observation upon which the model was tested was the redundancy in volatile organic compounds (VOC) found across plant species in a plant-herbivore community. Interestingly, Zu et al.’s model predicted successfully that VOC redundancy in the plant community associates with increased conditional entropy, which conveys herbivore confusion and plant protection against herbivory. In this way, plant species that evolve VOCs already present in the community might be benefitted, ultimately leading to the patterns of VOC redundancy commonly observed in nature.

Bass & Kessler performed a series of interesting observations on Zu et al. (2020), that can be organized along three lines of reasoning. First, from an evolutionary perspective, Bass & Kessler note the important point that accepting that conditional information entropy, estimated from the contribution of every plant species to volatile redundancy implies that average plant fitness seems to depend on community-level properties (i.e., what the other species in the community are doing) rather than on population-level characteristics (I.e., what the individuals belonging a population are doing). While the level at which selection acts upon is a longstanding debate (e.g., Goodnight, 1990; Williams, 1992), the model seems to contradict one of the basic tenets of Darwinian evolution. The extent to which this important observation invalidates the contribution of Zu et al. (2020) is open to scrutiny. However, one can indulge the evolutionary criticism by arguing that every theoretical model performs a number of assumptions to preserve the simplicity of analyses. Furthermore, even accepting the criticism, the overall information-based framework is valuable as it provides a fresh perspective to the way coding and decoding chemical information in plant-herbivore interactions may result in arm race coevolution. The question to be assessed by members of the scientific community is how strong the evolutionary assumptions are to be acceptable. A second line of reasoning involves consideration of additional routes of chemical information transfer. If chemical volatiles are involved in another ecological function unrelated to arm race (as they are) such as toxicity, crypsis, aposematism, etc., the conditional information indices considered as proxy to plant and herbivore fitness may be only secondarily related to arms race. This is an interesting observation, which suggests that VOC production may have more than one ecological function, as it often happens in “pleiotropic” traits (Strauss, Irwin 2004). This is an exciting avenue for future research. Finally, a third category of comments involves the relationship between conditional information entropy and plant and herbivore fitness. Bass & Kessler developed a Bayesian treatment of the community-level information developed by Zu et al. (2020) that permitted to estimate fitness on a species rather than community level. Their results revealed that community conditional entropies fail to align with species-level indices, suggesting that conclusions of Strauss & Irwin (2004) are not commensurate with fitness at the species level, where the analysis seems to be pertinent. In general, I strongly recommend Bass & Kessler’s contribution as it provides a series of observations and new perspectives to Zu et al. (2020). Rather than restricting their manuscript to blind criticisms, Bass & Kessler provides new interesting perspectives, which is always welcome as it improves the value and scope of the original work.

References

Bascompte J, Jordano P (2013) Mutualistic Networks. Princeton University Press. https://doi.org/10.23943/princeton/9780691131269.001.0001

Bass E, Kessler A (2022) Comment on “Information arms race explains plant-herbivore chemical communication in ecological communities.” EcoEvoRxiv, ver. 8 peer-reviewed and recommended by Peer Community in Ecology.  https://doi.org/10.32942/osf.io/xsbtm

Goodnight CJ (1990) Experimental Studies of Community Evolution I: The Response to Selection at the Community Level. Evolution, 44, 1614–1624. https://doi.org/10.1111/j.1558-5646.1990.tb03850.x

Schaefer HM, Ruxton GD (2011) Plant-Animal Communication. Oxford University Press, Oxford. https://doi.org/10.1093/acprof:osobl/9780199563609.001.0001

Strauss SY, Irwin RE (2004) Ecological and Evolutionary Consequences of Multispecies Plant-Animal Interactions. Annual Review of Ecology, Evolution, and Systematics, 35, 435–466. https://doi.org/10.1146/annurev.ecolsys.35.112202.130215

Williams GC (1992) Natural Selection: Domains, Levels, and Challenges. Oxford University Press, Oxford, New York.

Zu P, Boege K, del-Val E, Schuman MC, Stevenson PC, Zaldivar-Riverón A, Saavedra S (2020) Information arms race explains plant-herbivore chemical communication in ecological communities. Science, 368, 1377–1381. https://doi.org/10.1126/science.aba2965

A network includes a set of vertices or nodes (e.g., species in an interaction network), and a set of edges or links (e.g., interactions between species). Whether and how networks vary in space and/or time are questions often addressed in ecological research. 

Two ecological networks can differ in several extents: in that species are different in the two networks and establish new interactions (species turnover), or in that species that are present in both networks establish different interactions in the two networks (rewiring). The ecological meaning of changes in network structure is quite different according to whether species turnover or interaction rewiring plays a greater role. Therefore, much attention has been devoted in recent years on quantifying and interpreting the relative changes in network structure due to species turnover and/or rewiring.

Poisot et al. (2012) proposed to partition the global variation in structure between networks, \( \beta_{WN} \) (WN = Whole Network) into two terms: \( \beta_{OS} \) (OS = Only Shared species) and \( \beta_{ST} \) (ST = Species Turnover), such as \( \beta_{WN} = \beta_{OS} + \beta_{ST} \).

The calculation lays on enumerating the interactions between species that are common or not to two networks, as illustrated on Figure 1 for a simple case. Specifically, Poisot et al. (2012) proposed to use a Sorensen type measure of network dissimilarity, i.e., \( \beta_{WN} = \frac{a+b+c}{(2a+b+c)/2} -1=\frac{b+c}{2a+b+c} \) , where \( a \) is the number of interactions shared between the networks, while \( b \) and \( c \) are interaction numbers unique to one and the other network, respectively. \( \beta_{OS} \) is calculated based on the same formula, but only for the subnetworks including the species common to the two networks, in the form \( \beta_{OS} = \frac{b_{OS}+c_{OS}}{2a_{OS}+b_{OS}+c_{OS}} \) (e.g., Fig. 1). \( \beta_{ST} \) is deduced by subtracting \( \beta_{OS} \) from \( \beta_{WN} \) and represents in essence a "dissimilarity in interaction structure introduced by dissimilarity in species composition" (Poisot et al. 2012).

Figure 1. Ecological networks exemplified in Fründ (2021) and discussed in Poisot (2022). a is the number of shared links (continuous lines in right figures), while b+c is the number of edges unique to one or the other network (dashed lines in right figures).

Alternatively, Fründ (2021) proposed to define \( \beta_{OS} = \frac{b_{OS}+c_{OS}}{2a+b+c} \) and \( \beta_{ST} = \frac{b_{ST}+c_{ST}}{2a+b+c} \), where \( b_{ST}=b-b_{OS} \)  and \( c_{ST}=c-c_{OS} \) , so that the components \( \beta_{OS} \) and \( \beta_{ST} \) have the same denominator. In this way, Fründ (2021) partitioned the count of unique \( b+c=b_{OS}+b_{ST}+c_{ST} \) interactions, so that \( \beta_{OS} \) and \( \beta_{ST} \) sums to \( \frac{b_{OS}+c_{OS}+b_{ST}+c_{ST}}{2a+b+c} = \frac{b+c}{2a+b+c} = \beta_{WN} \). Fründ (2021) advocated that this partition allows a more sensible comparison of \( \beta_{OS} \) and \( \beta_{ST} \), in terms of the number of links that contribute to each component.

For instance, let us consider the networks 1 and 2 in Figure 1 (left panel) such as \( a_{OS}=2 \) (continuous lines in right panel), \( b_{ST} + c_{ST} = 1 \) and \( b_{OS} + c_{OS} = 1 \) (dashed lines in right panel), and thereby \( a = 2 \), \( b+c=2 \), \( \beta_{WN} = 1/3 \). Fründ (2021) measured \( \beta_{OS}=\beta_{ST}=1/6 \) and argued that it is appropriate insofar as it reflects that the number of unique links in the OS and ST components contributing to network dissimilarity (dashed lines) are actually equal. Conversely, the formula of Poisot et al. (2012) yields \( \beta_{OS}=1/5 \), hence \( \beta_{ST} = \frac{1}{3}-\frac{1}{5}=\frac{2}{15}<\beta_{OS} \). Fründ (2021) thus argued that the method of Poisot tends to underestimate the contribution of species turnover.

To clarify and avoid misinterpretation of the calculation of \( \beta_{OS} \) and \( \beta_{ST} \) in Poisot et al. (2012), Poisot (2022) provides a new, in-depth mathematical analysis of the decomposition of \( \beta_{WN} \). Poisot et al. (2012) quantify in \( \beta_{OS} \) the actual contribution of rewiring in network structure for the subweb of common species. Poisot (2022) thus argues that \( \beta_{OS} \) relates only to the probability of rewiring in the subweb, while the definition of \( \beta_{OS} \) by Fründ (2021) is relative to the count of interactions in the global network (considered in denominator), and is thereby dependent on both rewiring probability and species turnover. Poisot (2022) further clarifies the interpretation of \( \beta_{ST} \). \( \beta_{ST} \) is obtained by subtracting \( \beta_{OS} \) from \( \beta_{WN} \) and thus represents the influence of species turnover in terms of the relative architectures of the global networks and of the subwebs of shared species. Coming back to the example of Fig.1., the Poisot et al. (2012) formula posits that \( \frac{\beta_{ST}}{\beta_{WN}}=\frac{2/15}{1/3}=2/5 \), meaning that species turnover contributes two-fifths of change in network structure, while rewiring in the subweb of common species contributed three fifths.  Conversely, the approach of Fründ (2021) does not compare the architectures of global networks and of the subwebs of shared species, but considers the relative contribution of unique links to network dissimilarity in terms of species turnover and rewiring. 

Poisot (2022) concludes that the partition proposed in Fründ (2021) does not allow unambiguous ecological interpretation of rewiring. He provides guidelines for proper interpretation of the decomposition proposed in Poisot et al. (2012).

References

Fründ J (2021) Dissimilarity of species interaction networks: how to partition rewiring and species turnover components. Ecosphere, 12, e03653. https://doi.org/10.1002/ecs2.3653

Poisot T, Canard E, Mouillot D, Mouquet N, Gravel D (2012) The dissimilarity of species interaction networks. Ecology Letters, 15, 1353–1361. https://doi.org/10.1111/ele.12002

Poisot T (2022) Dissimilarity of species interaction networks: quantifying the effect of turnover and rewiring. EcoEvoRxiv Preprints, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/osf.io/gxhu2

There is growing evidence of worldwide decline of populations of top predators, including marine ones (Heithaus et al, 2008, Mc Cauley et al., 2015), with cascading effects expected at the ecosystem level, due to global change and human activities, including habitat loss or fragmentation, the collapse or the range shifts of their preys. On a global scale, seabirds are among the most threatened group of birds, about one-third of them being considered as threatened or endangered (Votier& Sherley, 2017). The large consequences of the decrease of the populations of preys they feed on (Cury et al, 2011) points diet flexibility as one important element to understand for effective management (McInnes et al, 2017).  Nevertheless, morphological inventory of preys requires intrusive protocols, and the differential digestion rate of distinct taxa may lead to a large bias in morphological-based diet assessments. The use of DNA metabarcoding on feces (or diet DNA, dDNA) now allows non-invasive approaches facilitating the recollection of samples and the detection of multiple preys independently of their digestion rates (Deagle et al., 2019). Although no gold standard exists yet to avoid bias associated with metabarcoding (primer bias, gaps in reference databases, inability to differentiate primary from secondary predation…), the use of these recent techniques has already improved the knowledge of the foraging behaviour and diet of many animals (Ando et al., 2020).

Both promise and shortcomings of this approach are illustrated in the article “Metabarcoding faecal samples to investigate spatiotemporal variation in the diet of the endangered Westland petrel (Procellaria westlandica)” by Quereteja et al. (2021). In this work, the authors assessed the nature and spatio-temporal flexibility of the foraging behaviour and consequent diet of the endangered petrel Procellaria westlandica from New-Zealand through metabarcoding of faeces samples.

The results of this dDNA, non-invasive approach, identify some expected and also unexpected prey items, some of which require further investigation likely due to large gaps in the reference databases. They also reveal the temporal (before and after hatching) and spatial (across colonies only 1.5km apart) flexibility of the foraging behaviour, additionally suggesting a possible influence of fisheries activities in the surroundings of the colonies. This study thus both underlines the power of the non-invasive metabarcoding approach on faeces, and the important results such analysis can deliver for conservation, pointing a potential for diet flexibility that may be essential for the resilience of this iconic yet endangered species.

References

Ando H, Mukai H, Komura T, Dewi T, Ando M, Isagi Y (2020) Methodological trends and perspectives of animal dietary studies by noninvasive fecal DNA metabarcoding. Environmental DNA, 2, 391–406. https://doi.org/10.1002/edn3.117

Cury PM, Boyd IL, Bonhommeau S, Anker-Nilssen T, Crawford RJM, Furness RW, Mills JA, Murphy EJ, Österblom H, Paleczny M, Piatt JF, Roux J-P, Shannon L, Sydeman WJ (2011) Global Seabird Response to Forage Fish Depletion—One-Third for the Birds. Science, 334, 1703–1706. https://doi.org/10.1126/science.1212928

Deagle BE, Thomas AC, McInnes JC, Clarke LJ, Vesterinen EJ, Clare EL, Kartzinel TR, Eveson JP (2019) Counting with DNA in metabarcoding studies: How should we convert sequence reads to dietary data? Molecular Ecology, 28, 391–406. https://doi.org/10.1111/mec.14734

Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution, 23, 202–210. https://doi.org/10.1016/j.tree.2008.01.003

McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR (2015) Marine defaunation: Animal loss in the global ocean. Science, 347, 1255641. https://doi.org/10.1126/science.1255641

McInnes JC, Jarman SN, Lea M-A, Raymond B, Deagle BE, Phillips RA, Catry P, Stanworth A, Weimerskirch H, Kusch A, Gras M, Cherel Y, Maschette D, Alderman R (2017) DNA Metabarcoding as a Marine Conservation and Management Tool: A Circumpolar Examination of Fishery Discards in the Diet of Threatened Albatrosses. Frontiers in Marine Science, 4, 277. https://doi.org/10.3389/fmars.2017.00277

Querejeta M, Lefort M-C, Bretagnolle V, Boyer S (2021) Metabarcoding faecal samples to investigate spatiotemporal variation in the diet of the endangered Westland petrel (Procellaria westlandica). bioRxiv, 2020.10.30.360289, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2020.10.30.360289

Votier SC, Sherley RB (2017) Seabirds. Current Biology, 27, R448–R450. https://doi.org/10.1016/j.cub.2017.01.042

Ecology is the study of the distribution of organisms in space and time and their interactions. As such, there is a tradition of studies relating abiotic environmental conditions to species distribution, while another one is concerned by the effects of consumers on the abundance of their resources.  Interestingly, joining the dots appears more difficult than it would suggest: eluding the effect of species interactions on distribution remains one of the greatest challenges to elucidate nowadays (Kissling et al. 2012). Theory suggests that yes, species interactions such as predation and competition should influence range limits (Godsoe et al. 2017), but the common intuition among many biogeographers remains that over large areas such as regions and continents, environmental drivers like temperature and precipitation overwhelm their local effects. Answering this question is of primary importance in the context where species are moving around with climate warming.  Inconsistencies in food web structure may arise with asynchronized movements of consumers and their resources, leading to a major disruption in regulation and potentially ecosystem functioning. Solving this problem, however, remains very challenging because we have to rely on observational data since experiments are hard to perform at the biogeographical scale. 

The study of St-Gelais is an interesting step forward to solve this problem. Their main objective was to assess the strength of the association between phytoplankton and zooplankton communities at a large spatial scale, looking at the spatial covariation of both taxonomic and functional composition. To do so, they undertook a massive survey of more than 100 lakes across three regions of the boreal region of Québec. Species and functional composition were recorded, along with a set of abiotic variables. Classic community ecology at this point. The difficulty they faced was to disentangle the multiple causal relationships involved in the distribution of both trophic levels. Teasing apart bottom-up and top-down forces driving the assembly of plankton communities using observational data is not an easy task. On the one hand, both trophic levels could respond to variations in temperature, nutrient availability and dissolved organic carbon. The interpretation is fairly straightforward if the two levels respond to different factors, but the situation is much more complicated when they do respond similarly. There are potentially three possible underlying scenarios. First, the phyto and zooplankton communities may share the same environmental requirements, thereby generating a joint distribution over gradients such as temperature and nutrient availability. Second, the abiotic environment could drive the distribution of the phytoplankton community, which would then propagate up and influence the distribution of the zooplankton community. Alternatively, the abiotic environment could constrain the distribution of the zooplankton, which could then affect the one of phytoplankton. In addition to all of these factors, St-Gelais et al also consider that dispersal may limit the distribution, well aware of previous studies documenting stronger dispersal limitations for zooplankton communities. 

Unfortunately, there is not a single statistical approach that could be taken from the shelf and used to elucidate drivers of co-distribution. Joint species distribution was once envisioned as a major step forward in this direction (Warton et al. 2015), but there are several limits preventing the direct interpretation that co-occurrence is linked to interactions (Blanchet et al. 2020). Rather, St-Gelais used a variety of multivariate statistics to reveal the structure in their observational data. First, using a Procrustes analysis (a method testing if the spatial variation of one community is correlated to the structure of another community), they found a significant correlation between phytoplankton and zooplankton communities, indicating a taxonomic coupling between the groups. Interestingly, this observation was maintained for functional composition only when interaction-related traits were considered. At this point, these results strongly suggest that interactions are involved in the correlation, but it's hard to decipher between bottom-up and top-down perspectives. A complementary analysis performed with a constrained ordination, per trophic level, provided complementary pieces of information. First observation was that only functional variation was found to be related to the different environmental variables, not taxonomic variation. Despite that trophic levels responded to water quality variables, spatial autocorrelation was more important for zooplankton communities and the two layers appear to respond to different variables. 

It is impossible with those results to formulate a strong conclusion about whether grazing influence the co-distribution of phytoplankton and zooplankton communities. That's the mere nature of observational data. While there is a strong spatial association between them, there are also diverging responses to the different environmental variables considered. But the contrast between taxonomic and functional composition is nonetheless informative and it seems that beyond the idiosyncrasies of species composition, trait distribution may be more informative and general. Perhaps the most original contribution of this study is the hierarchical approach to analyze the data, combined with the simultaneous analysis of taxonomic and functional distributions. Having access to a vast catalog of multivariate statistical techniques, a careful selection of analyses helps revealing key features in the data, rejecting some hypotheses and accepting others. Hopefully, we will see more and more of such multi-trophic approaches to distribution because it is now clear that the factors driving distribution are much more complicated than anticipated in more traditional analyses of community data. Biodiversity is more than a species list, it is also all of the interactions between them, influencing their distribution and abundance (Jordano 2016).

References

Blanchet FG, Cazelles K, Gravel D (2020) Co-occurrence is not evidence of ecological interactions. Ecology Letters, 23, 1050–1063. https://doi.org/10.1111/ele.13525

Godsoe W, Jankowski J, Holt RD, Gravel D (2017) Integrating Biogeography with Contemporary Niche Theory. Trends in Ecology & Evolution, 32, 488–499. https://doi.org/10.1016/j.tree.2017.03.008

Jordano P (2016) Chasing Ecological Interactions. PLOS Biology, 14, e1002559. https://doi.org/10.1371/journal.pbio.1002559

Kissling WD, Dormann CF, Groeneveld J, Hickler T, Kühn I, McInerny GJ, Montoya JM, Römermann C, Schiffers K, Schurr FM, Singer A, Svenning J-C, Zimmermann NE, O’Hara RB (2012) Towards novel approaches to modelling biotic interactions in multispecies assemblages at large spatial extents. Journal of Biogeography, 39, 2163–2178. https://doi.org/10.1111/j.1365-2699.2011.02663.x

St-Gelais NF, Vogt RJ, Giorgio PA del, Beisner BE (2021) The taxonomic and functional biogeographies of phytoplankton and zooplankton communities across boreal lakes. bioRxiv, 373332, ver. 4 peer-reviewed and recommended by Peer community in Ecology. https://doi.org/10.1101/373332

Warton DI, Blanchet FG, O’Hara RB, Ovaskainen O, Taskinen S, Walker SC, Hui FKC (2015) So Many Variables: Joint Modeling in Community Ecology. Trends in Ecology & Evolution, 30, 766–779. https://doi.org/10.1016/j.tree.2015.09.007

Wisz MS, Pottier J, Kissling WD, Pellissier L, Lenoir J, Damgaard CF, Dormann CF, Forchhammer MC, Grytnes J-A, Guisan A, Heikkinen RK, Høye TT, Kühn I, Luoto M, Maiorano L, Nilsson M-C, Normand S, Öckinger E, Schmidt NM, Termansen M, Timmermann A, Wardle DA, Aastrup P, Svenning J-C (2013) The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modelling. Biological Reviews, 88, 15–30. https://doi.org/10.1111/j.1469-185X.2012.00235.x

Alarm calls are an important acoustic signal that can decide the life or death of an individual. Many birds are able to vary their alarm calls to provide more accurate information on e.g. urgency or even the type of a threatening predator. According to the acoustic adaptation hypothesis, the habitat plays an important role too in how acoustic patterns get transmitted. This is of particular interest for range-expanding species that will face new environmental conditions along the leading edge. One could hypothesize that the alarm call repertoire of a species could increase in newly founded ranges to incorporate new habitats and threats individuals might face. Hence selection for a larger active vocabulary might be beneficial for new colonizers. Using the Great-Tailed Grackle (Quiscalus mexicanus) as a model species, Samantha Bowser from Arizona State University and Maggie MacPherson from Louisiana State University want to find out exactly that. 

The Great-Tailed Grackle is an appropriate species given its high vocal diversity. Also, the species consists of different subspecies that show range expansions along the northern range edge yet to a varying degree. Using vocal experiments and field recordings the researchers have a high potential to understand more about the acoustic adaptation hypothesis within a range dynamic process. 

Over the course of this assessment, the authors incorporated the comments made by two reviewers into a strong revision of their research plans. With that being said, the few additional comments made by one of the initial reviewers round up the current stage this interesting research project is in. 

To this end, I can only fully recommend the revised research plan and am much looking forward to the outcomes from the author’s experiments, modeling, and field data. With the suggestions being made at such an early stage I firmly believe that the final outcome will be highly interesting not only to an ornithological readership but to every ecologist and biogeographer interested in drivers of range dynamic processes.

References

Bowser, S., MacPherson, M. (2021). A study on the role of social information sharing leading to range expansion in songbirds with large vocal repertoires: Enhancing our understanding of the Great-Tailed Grackle (Quiscalus mexicanus) alarm call. In principle recommendation by PCI Ecology. https://doi.org/10.17605/OSF.IO/2UFJ5. Version 3