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13 May 2023
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Symbiotic nutrient cycling enables the long-term survival of Aiptasia in the absence of heterotrophic food sources

Constraining the importance of heterotrophic vs autotrophic feeding in photosymbiotic cnidarians

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

The symbiosis with autotrophic dinoflagellate algae has enabled heterotrophic Cnidaria to thrive in nutrient-poor tropical waters (Muscatine and Porter 1977; Stanley 2006). In particular, mixotrophy, i.e. the ability to acquire nutrients through both autotrophy and heterotrophy, confers a competitive edge in oligotrophic waters, allowing photosymbiotic Cnidaria to outcompete benthic organisms limited to a single diet (e.g., McCook 2001). However, the relative importance of autotrophy vs heterotrophy in sustaining symbiotic cnidarian’s nutrition is still the subject of intense research. In fact, figuring out the cellular mechanisms by which symbiotic Cnidaria acquire a balanced diet for their metabolism and growth is relevant to our understanding of their physiology under varying environmental conditions and in response to anthropogenic perturbations.

In this study's long-term starvation experiment, Radecker & Meibom (2023) investigated the survival of the photosymbiotic sea anemone Aiptasia in the absence of heterotrophic feeding. After one year of heterotrophic starvation, Apitasia anemones remained fully viable but showed an 85 % reduction in biomass. Using 13C-bicarbonate and 15N-ammonium labeling, electron microscopy and NanoSIMS imaging, the authors could clearly show that the contribution of algal-derived nutrients to the host metabolism remained unaffected as a result of increased algal photosynthesis and more efficient carbon translocation. At the same time, the absence of heterotrophic feeding caused severe nitrogen limitation in the starved Apitasia anemones.

Overall, this study provides valuable insights into nutrient exchange within the symbiosis between Cnidaria and dinoflagellate algae at the cellular level and sheds new light on the importance of heterotrophic feeding as a nitrogen acquisition strategy for holobiont growth in oligotrophic waters.

REFERENCES

McCook L (2001) Competition between corals and algal turfs along a gradient of terrestrial influence in the nearshore central Great Barrier Reef. Coral Reefs 19:419–425. https://doi.org/10.1007/s003380000119

Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460. https://doi.org/10.2307/1297526

Radecker N, Meibom A (2023) Symbiotic nutrient cycling enables the long-term survival of Aiptasia in the absence of heterotrophic food sources. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.12.07.519152

Stanley GD Jr (2006) Photosymbiosis and the evolution of modern coral reefs. Science 312:857–858. https://doi.org/10.1126/science.1123701

Symbiotic nutrient cycling enables the long-term survival of Aiptasia in the absence of heterotrophic food sourcesNils Radecker, Anders Meibom<p style="text-align: justify;">Phototrophic Cnidaria are mixotrophic organisms that can complement their heterotrophic diet with nutrients assimilated by their algal endosymbionts. Metabolic models suggest that the translocation of photosynthates...Eco-evolutionary dynamics, Microbial ecology & microbiology, SymbiosisUlisse Cardini2022-12-12 10:50:55 View
29 Mar 2021
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Temperature predicts the maximum tree-species richness and water and frost shape the residual variation

New light on the baseline importance of temperature for the origin of geographic species richness gradients

Recommended by based on reviews by Rafael Molina-Venegas and 2 anonymous reviewers

Whether environmental conditions –in particular energy and water availability– are sufficient to account for species richness gradients (e.g. Currie 1991), or the effects of other biotic and historical or regional factors need to be considered as well (e.g. Ricklefs 1987), was the subject of debate during the 1990s and 2000s (e.g. Francis & Currie 2003; Hawkins et al. 2003, 2006; Currie et al. 2004; Ricklefs 2004). The metabolic theory of ecology (Brown et al. 2004) provided a solid and well-rooted theoretical support for the preponderance of energy as the main driver for richness variations. As any good piece of theory, it provided testable predictions about the sign and shape (i.e. slope) of the relationship between temperature –a key aspect of ambient energy– and species richness. However, these predictions were not supported by empirical evaluations (e.g. Kreft & Jetz 2007; Algar et al. 2007; Hawkins et al. 2007a), as the effects of a myriad of other environmental gradients, regional factors and evolutionary processes result in a wide variety of richness–temperature responses across different groups and regions (Hawkins et al. 2007b; Hortal et al. 2008). So, in a textbook example of how good theoretical work helps advancing science even if proves to be (partially) wrong, the evaluation of this aspect of the metabolic theory of ecology led to current understanding that, while species richness does respond to current climatic conditions, many other ecological, evolutionary and historical factors do modify such response across scales (see, e.g., Ricklefs 2008; Hawkins 2008; D’Amen et al. 2017). And the kinetic model linking mean annual temperature and species richness (Allen et al. 2002; Brown et al. 2004) was put aside as being, perhaps, another piece of the puzzle of the origin of current diversity gradients.

Segovia (2021) puts together an elegant way of reinvigorating this part of the metabolic theory of ecology. He uses quantile regressions to model just the upper parts of the relationship between species richness and mean annual temperature, rather than modelling its central tendency through the classical linear regression family of methods –as was done in the past. This assumes that the baseline effect of ambient energy does produce the negative linear relationship between richness and temperature predicted by the kinetic model (Allen et al. 2002), but also that this effect only poses an upper limit for species richness, and the effects of other factors may result in lower levels of species co-occurrence, thus producing a triangular rather than linear relationship. The results of Segovia’s simple and elegant analytical design show unequivocally that the predictions of the kinetic model become progressively more explanatory towards the upper quartiles of the relationship between species richness and temperature along over 10,000 tree local inventories throughout the Americas, reaching over 70% of explanatory power for the upper 5% of the relationship (i.e. the 95% quantile). This confirms to a large extent his reformulation of the predictions of the kinetic model. 

Further, the neat study from Segovia (2021) also provides evidence confirming that the well-known spatial non-stationarity in the richness–temperature relationship (see Cassemiro et al. 2007) also applies to its upper-bound segment. Both the explanatory power and the slope of the relationship in the 95% upper quantile vary widely between biomes, reaching values similar to the predictions of the kinetic model only in cold temperate environments ­–precisely where temperature becomes more important than water availability as a constrain to plant life (O’Brien 1998; Hawkins et al. 2003). Part of these variations are indeed related with changes in water deficit and number of frost days along the XXth Century, as shown by the residuals of this paper (Segovia 2021) and a more detailed separate study (Segovia et al. 2020). This pinpoints the importance of the relative balance between water and energy as two of the main climatic factors constraining species diversity gradients, confirming the value of hypotheses that date back to Humboldt’s work (see Hawkins 2001, 2008). There is however a significant amount of unexplained variation in Segovia’s analyses, in particular in the progressive departure of the predictions of the kinetic model as we move towards the tropics, or downwards along the lower quantiles of the richness–temperature relationship. This calls for a deeper exploration of the factors that modify the baseline relationship between richness and energy, opening a new avenue for the macroecological investigation of how different forces and processes shape up geographical diversity gradients beyond the mere energetic constrains imposed by the basal limitations of multicellular life on Earth.

References

Algar, A.C., Kerr, J.T. and Currie, D.J. (2007) A test of Metabolic Theory as the mechanism underlying broad-scale species-richness gradients. Global Ecology and Biogeography, 16, 170-178. doi: https://doi.org/10.1111/j.1466-8238.2006.00275.x

Allen, A.P., Brown, J.H. and Gillooly, J.F. (2002) Global biodiversity, biochemical kinetics, and the energetic-equivalence rule. Science, 297, 1545-1548. doi: https://doi.org/10.1126/science.1072380

Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M. and West, G.B. (2004) Toward a metabolic theory of ecology. Ecology, 85, 1771-1789. doi: https://doi.org/10.1890/03-9000

Cassemiro, F.A.d.S., Barreto, B.d.S., Rangel, T.F.L.V.B. and Diniz-Filho, J.A.F. (2007) Non-stationarity, diversity gradients and the metabolic theory of ecology. Global Ecology and Biogeography, 16, 820-822. doi: https://doi.org/10.1111/j.1466-8238.2007.00332.x

Currie, D.J. (1991) Energy and large-scale patterns of animal- and plant-species richness. The American Naturalist, 137, 27-49. doi: https://doi.org/10.1086/285144

Currie, D.J., Mittelbach, G.G., Cornell, H.V., Field, R., Guegan, J.-F., Hawkins, B.A., Kaufman, D.M., Kerr, J.T., Oberdorff, T., O'Brien, E. and Turner, J.R.G. (2004) Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness. Ecology Letters, 7, 1121-1134. doi: https://doi.org/10.1111/j.1461-0248.2004.00671.x

D'Amen, M., Rahbek, C., Zimmermann, N.E. and Guisan, A. (2017) Spatial predictions at the community level: from current approaches to future frameworks. Biological Reviews, 92, 169-187. doi: https://doi.org/10.1111/brv.12222

Francis, A.P. and Currie, D.J. (2003) A globally consistent richness-climate relationship for Angiosperms. American Naturalist, 161, 523-536. doi: https://doi.org/10.1086/368223

Hawkins, B.A. (2001) Ecology's oldest pattern? Trends in Ecology & Evolution, 16, 470. doi: https://doi.org/10.1016/S0169-5347(01)02197-8 

Hawkins, B.A. (2008) Recent progress toward understanding the global diversity gradient. IBS Newsletter, 6.1, 5-8. https://escholarship.org/uc/item/8sr2k1dd

Hawkins, B.A., Field, R., Cornell, H.V., Currie, D.J., Guégan, J.-F., Kaufman, D.M., Kerr, J.T., Mittelbach, G.G., Oberdorff, T., O'Brien, E., Porter, E.E. and Turner, J.R.G. (2003) Energy, water, and broad-scale geographic patterns of species richness. Ecology, 84, 3105-3117. doi: https://doi.org/10.1890/03-8006

Hawkins, B.A., Diniz-Filho, J.A.F., Jaramillo, C.A. and Soeller, S.A. (2006) Post-Eocene climate change, niche conservatism, and the latitudinal diversity gradient of New World birds. Journal of Biogeography, 33, 770-780. doi: https://doi.org/10.1111/j.1365-2699.2006.01452.x

Hawkins, B.A., Albuquerque, F.S., Araújo, M.B., Beck, J., Bini, L.M., Cabrero-Sañudo, F.J., Castro Parga, I., Diniz-Filho, J.A.F., Ferrer-Castán, D., Field, R., Gómez, J.F., Hortal, J., Kerr, J.T., Kitching, I.J., León-Cortés, J.L., et al. (2007a) A global evaluation of metabolic theory as an explanation for terrestrial species richness gradients. Ecology, 88, 1877-1888. doi:10.1890/06-1444.1. doi: https://doi.org/10.1890/06-1444.1

Hawkins, B.A., Diniz-Filho, J.A.F., Bini, L.M., Araújo, M.B., Field, R., Hortal, J., Kerr, J.T., Rahbek, C., Rodríguez, M.Á. and Sanders, N.J. (2007b) Metabolic theory and diversity gradients: Where do we go from here? Ecology, 88, 1898–1902. doi: https://doi.org/10.1890/06-2141.1

Hortal, J., Rodríguez, J., Nieto-Díaz, M. and Lobo, J.M. (2008) Regional and environmental effects on the species richness of mammal assemblages. Journal of Biogeography, 35, 1202–1214. doi: https://doi.org/10.1111/j.1365-2699.2007.01850.x

Kreft, H. and Jetz, W. (2007) Global patterns and determinants of vascular plant diversity. Proceedings of the National Academy of Sciences USA, 104, 5925-5930. doi: https://doi.org/10.1073/pnas.0608361104

O'Brien, E. (1998) Water-energy dynamics, climate, and prediction of woody plant species richness: an interim general model. Journal of Biogeography, 25, 379-398. doi: https://doi.org/10.1046/j.1365-2699.1998.252166.x

Ricklefs, R.E. (1987) Community diversity: Relative roles of local and regional processes. Science, 235, 167-171. doi: https://doi.org/10.1126/science.235.4785.167

Ricklefs, R.E. (2004) A comprehensive framework for global patterns in biodiversity. Ecology Letters, 7, 1-15. doi: https://doi.org/10.1046/j.1461-0248.2003.00554.x

Ricklefs, R.E. (2008) Disintegration of the ecological community. American Naturalist, 172, 741-750. doi: https://doi.org/10.1086/593002

Segovia, R.A. (2021) Temperature predicts the maximum tree-species richness and water and frost shape the residual variation. bioRxiv, 836338, ver. 4 peer-reviewed and recommended by Peer community in Ecology. doi: https://doi.org/10.1101/836338

Segovia, R.A., Pennington, R.T., Baker, T.R., Coelho de Souza, F., Neves, D.M., Davis, C.C., Armesto, J.J., Olivera-Filho, A.T. and Dexter, K.G. (2020) Freezing and water availability structure the evolutionary diversity of trees across the Americas. Science Advances, 6, eaaz5373. doi: https://doi.org/10.1126/sciadv.aaz5373

Temperature predicts the maximum tree-species richness and water and frost shape the residual variationRicardo A. Segovia<p>The kinetic hypothesis of biodiversity proposes that temperature is the main driver of variation in species richness, given its exponential effect on biological activity and, potentially, on rates of diversification. However, limited support fo...Biodiversity, Biogeography, Botany, Macroecology, Species distributionsJoaquín Hortal2019-11-10 20:56:40 View
31 Oct 2022
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Ten simple rules for working with high resolution remote sensing data

Preventing misuse of high-resolution remote sensing data

Recommended by ORCID_LOGO based on reviews by Jane Wyngaard and 1 anonymous reviewer

To observe, characterise, identify, understand, predict... This is the approach that researchers follow every day. This sequence is tirelessly repeated as the biological model, the targeted ecosystem and/or the experimental, environmental or modelling conditions change. This way of proceeding is essential in a world of rapid change in response to the frenetic pace of intensifying pressures and forcings that impact ecosystems. To better understand our Earth and the dynamics of its components, to map ecosystems and diversity patterns, and to identify changes, humanity had to demonstrate inventiveness and defy gravity. 

Gustave Hermite and Georges Besançon were the first to launch aloft balloons equipped with radio transmitters, making possible the transmission of meteorological data to observers in real time [1]. The development of aviation in the middle of the 20th century constituted a real leap forward for the frequent acquisition of aerial observations, leading to a significant improvement in weather forecasting models. The need for systematic collection of data as holistic as possible – an essential component for the observation of complex biological systems - has resulted in pushing the limits of technological prowess. 

The conquest of space and the concurrent development of satellite observations has largely contributed to the collection of a considerable mass of data, placing our Earth under the "macroscope" - a concept introduced to ecology in the early 1970s by Howard T. Odum (see [2]), and therefore allowing researchers to move towards a better understanding of ecological systems, deterministic and stochastic patterns … with the ultimate goal of improving management actions [2,3]. Satellite observations have been carried out for nearly five decades now [3] and have greatly contributed to a better qualitative and quantitative understanding of the functioning of our planet, its diversity, its climate... and to a better anticipation of possible future changes (e.g., [4-7]).

This access to rich and complex sources of information, for which both spatial and temporal resolutions are increasingly fine, results in the implementation of increasingly complex computation-based analyses, in order to meet the need for a better understanding of ecological mechanisms and processes, and their possible changes. Steven Levitt stated that "Data is one of the most powerful mechanisms for telling stories". This is so true … Data should not be used as a guide to thinking and a critical judgment at each stage of the data exploitation process should not be neglected. 

This is what Mahood et al. [8] rightly remind us in their article "Ten simple rules for working with high-resolution remote sensing data" in which they provide the fundamentals to consider when working with data of this nature, a still underutilized resource in several topics, such as conservation biology [3]. In this unconventional article, presented in a pedagogical way, the authors remind different generations of readers how satellite data should be handled and processed. The authors aim to make the readers aware of the most frequent pitfalls encouraging them to use data adapted to their original question, the most suitable tools/methods/procedures, to avoid methodological overkill, and to ensure both ethical use of data and transparency in the research process. While access to high-resolution data is increasingly easy thanks to the implementation of dedicated platforms [4], and because of the development of easy-to-use processing software and pipelines, it is important to take the time to recall some of the essential rules and guidelines for managing them, from new users with little or no experience who will find in this article the recommendations, resources and advice necessary to start exploiting remote sensing data, to more experienced researchers.

References

[1] Jeannet P, Philipona R, and Richner H (2016). 8 Swiss upper-air balloon soundings since 1902. In: Willemse S, Furger M (2016) From weather observations to atmospheric and climate sciences in Switzerland: Celebrating 100 years of the Swiss Society for Meteorology. vdf Hochschulverlag AG. 

[2] Odum HT (2007) Environment, Power, and Society for the Twenty-First Century: The Hierarchy of Energy. Columbia University Press.

[3] Boyle SA, Kennedy CM, Torres J, Colman K, Pérez-Estigarribia PE, Sancha NU de la (2014) High-Resolution Satellite Imagery Is an Important yet Underutilized Resource in Conservation Biology. PLOS ONE, 9, e86908. https://doi.org/10.1371/journal.pone.0086908

[4] Le Traon P-Y, Antoine D, Bentamy A, Bonekamp H, Breivik LA, Chapron B, Corlett G, Dibarboure G, DiGiacomo P, Donlon C, Faugère Y, Font J, Girard-Ardhuin F, Gohin F, Johannessen JA, Kamachi M, Lagerloef G, Lambin J, Larnicol G, Le Borgne P, Leuliette E, Lindstrom E, Martin MJ, Maturi E, Miller L, Mingsen L, Morrow R, Reul N, Rio MH, Roquet H, Santoleri R, Wilkin J (2015) Use of satellite observations for operational oceanography: recent achievements and future prospects. Journal of Operational Oceanography, 8, s12–s27. https://doi.org/10.1080/1755876X.2015.1022050

[5] Turner W, Rondinini C, Pettorelli N, Mora B, Leidner AK, Szantoi Z, Buchanan G, Dech S, Dwyer J, Herold M, Koh LP, Leimgruber P, Taubenboeck H, Wegmann M, Wikelski M, Woodcock C (2015) Free and open-access satellite data are key to biodiversity conservation. Biological Conservation, 182, 173–176. https://doi.org/10.1016/j.biocon.2014.11.048

[6] Melet A, Teatini P, Le Cozannet G, Jamet C, Conversi A, Benveniste J, Almar R (2020) Earth Observations for Monitoring Marine Coastal Hazards and Their Drivers. Surveys in Geophysics, 41, 1489–1534. https://doi.org/10.1007/s10712-020-09594-5

[7] Zhao Q, Yu L, Du Z, Peng D, Hao P, Zhang Y, Gong P (2022) An Overview of the Applications of Earth Observation Satellite Data: Impacts and Future Trends. Remote Sensing, 14, 1863. https://doi.org/10.3390/rs14081863

[8] Mahood AL, Joseph MB, Spiers A, Koontz MJ, Ilangakoon N, Solvik K, Quarderer N, McGlinchy J, Scholl V, Denis LS, Nagy C, Braswell A, Rossi MW, Herwehe L, Wasser L, Cattau ME, Iglesias V, Yao F, Leyk S, Balch J (2021) Ten simple rules for working with high resolution remote sensing data. OSFpreprints, ver. 6 peer-reviewed and recommended by Peer Community in Ecology.  https://doi.org/10.31219/osf.io/kehqz

Ten simple rules for working with high resolution remote sensing dataAdam L. Mahood, Maxwell Benjamin Joseph, Anna Spiers, Michael J. Koontz, Nayani Ilangakoon, Kylen Solvik, Nathan Quarderer, Joe McGlinchy, Victoria Scholl, Lise St. Denis, Chelsea Nagy, Anna Braswell, Matthew W. Rossi, Lauren Herwehe, Leah wasser,...<p>Researchers in Earth and environmental science can extract incredible value from high-resolution (sub-meter, sub-hourly or hyper-spectral) remote sensing data, but these data can be difficult to use. Correct, appropriate and competent use of su...Biogeography, Landscape ecology, Macroecology, Spatial ecology, Metacommunities & Metapopulations, Terrestrial ecologyEric Goberville2021-10-19 21:41:22 View
15 Nov 2023
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The challenges of independence: ontogeny of at-sea behaviour in a long-lived seabird

On the road to adulthood: exploring progressive changes in foraging behaviour during post-fledging immaturity using remote tracking

Recommended by based on reviews by Juliet Lamb and 1 anonymous reviewer

In most vertebrate species, the period of life spanning from departure from the growing site until reaching a more advanced life stage (immature or adult) is critical. During this period, juveniles are often highly vulnerable because they have not reached the morphological, physiological and behavioural maturity levels of adults yet and are therefore at high risk of mortality, e.g. through starvation, depredation or competition (e.g. Marchetti & Price 1989, Wunderle 1991, Naef-Daenzer & Grüebler 2016). In line with this, juvenile survival is most often far lower than adult survival (e.g. Wooller et al. 1992). In species with parental care, juveniles have to acquire behavioural independence from their parents and possibly establish their own territory during this period of life. Very often, this is also the period that is least well-known in the life cycle (Cox et al. 2014, Naef-Daenzer & Grüebler 2016) because of reduced accessibility to individuals and/or adoption of low conspicuous behaviours. Therefore, our understanding of how juveniles acquire typical adult behaviours and how this progressively increases their survival prospects is still very limited (Naef-Daenzer & Grüebler 2016), and questions such as the length of this transition period or the cognitive (e.g. learning, memorization) mechanisms involved remain largely unresolved. This is particularly true regarding the acquisition of independent foraging behaviour (Marchetti & Price 1989).

Because direct observations of juvenile behaviours are usually very difficult except in specific situations or at the cost of an enormous effort, the use of remote tracking devices can be particularly appealing in this context (e.g. Ponchon et al. 2013, Kays et al. 2015). Over the past decades, technical advances have allowed the monitoring of not only individuals’ movements at both large and small spatial scales but also their activities and behaviours based on different parameters recording e.g. speed of movement or diving depth (Whitford & Klimley 2019). Device miniaturization has in particular allowed smaller species to be equipped and/or longer periods of time to be monitored (e.g. Naef-Daenzer et al. 2005). This has opened up whole fields of research, and has been particularly used on marine seabirds. In these species, individuals are most often inaccessible when at sea, representing most of the time outside (and even within) the breeding season, and the life cycle of these long-lived species can include an extended immature period (up to many years) during which most of them will remain unseen, until they come back as breeders or pre-breeders (e.g. Wooller et al. 1992, Oro & Martínez-Abraín 2009). Survival has been found to increase gradually with age in these species before reaching high values characteristic of the adult stage. However, the mechanisms underlying this increase are still to be deciphered.

The study by Delord et al. (2023) builds upon the hypothesis that juveniles gradually learn foraging techniques and movement strategies, improving their foraging efficiency, as previous data on flight parameters seemed to show in different long-lived bird species. Yet, these previous studies obtained data over a limited period of time, i.e. a few months at best. Whether these data could capture the whole dynamics of the progressive acquisition of foraging and movement skills can only be assessed by measuring behaviour over a longer time period and comparing it to similar data in adults, to account for seasonal variation in relation to both resource availability and energetic demands, e.g. due to molt.

The present study (Delord et al. 2023) addresses these questions by taking advantage of longer-lasting recordings of the location and activity of juvenile, immature and adult birds obtained simultaneously to investigate changes over time in juvenile behaviour and thereby provide hints about how young progressively acquire foraging skills. This study is performed on Amsterdam albatrosses, a highly endangered long-lived sea bird, with obvious conservation issues (Thiebot et al. 2015). The results show progressive changes in foraging effort over the first two months after departure from the birth colony, but large differences remain between life stages over a much longer time frame. They also reveal strong variations between sexes and over time in the year. Overall, this study, therefore, confirms the need for very long-term data to be collected in order to address the question of progressive behavioural maturation and associated survival consequences in such species with strongly deferred maturity. Ideally, the same individuals should be monitored over different life stages, from the juvenile period up to adulthood, but this would require further technical development to release the issue of powering duration limitation.

As reviewers emphasized in the first review round, one main challenge now remains to ascertain the outcome of the observed behavioural changes in foraging behaviour: we expect them to reflect improvement in foraging skills and thus performance of juveniles over time, but this would need to be tested. Collecting data on foraging efficiency is yet another challenge, that future technical developments may also help overcome. Importantly also, data were available only for individuals that could be caught again because the tracking device had to be retrieved from the bird. Here, a substantial fraction of the loggers (one-fifth) could not be found again (Delord et al. 2023). To what extent the birds for which no data could be obtained are a random sample of the equipped birds would also need to be assessed. The further development of remote tracking techniques allowing data to be downloaded from a long distance should help further exploration of behavioural ontogeny of juveniles while maturing and its survival consequences. Because the maturation process explored here is likely to show very different characteristics (e.g. timing and speed) in smaller / shorter-lived species (see Cox et al. 2014, Naef-Daenzer & Grüebler 2016), the development of miniaturization is also expected to allow further investigation of post-fledging behavioural maturation in a wider range of bird species. Our understanding of this crucial life phase in different types of species should thus continue to progress in the coming years.

References

Cox W. A., Thompson F. R. III, Cox A. S. & Faaborg J. 2014. Post-fledging survival in passerine birds and the value of post-fledging studies to conservation. Journal of Wildlife Management, 78: 183-193. https://doi.org/10.1002/jwmg.670

Delord K., Weimerskirch H. & Barbraud C. 2023. The challenges of independence: ontogeny of at-sea behaviour in a long-lived seabird. bioRxiv, ver. 6 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2021.10.23.465439

Kays R., Crofoot M. C., Jetz W. & Wikelski M. 2015. Terrestrial animal tracking as an eye on life and planet. Science, 348 (6240). https://doi.org/10.1126/science.aaa2478

Marchetti K: & Price T. 1989. Differences in the foraging of juvenile and adult birds: the importance of developmental constraints. Biological Reviews, 64: 51-70. https://doi.org/10.1111/j.1469-185X.1989.tb00638.x

Naef-Daenzer B., Fruh D., Stalder M., Wetli P. & Weise E. 2005. Miniaturization (0.2 g) and evaluation of attachment techniques of telemetry transmitters. The Journal of Experimental Biology, 208: 4063–4068. https://doi.org/10.1242/jeb.01870

Naef-Daenzer B. & Grüebler M. U. 2016. Post-fledging survival of altricial birds: ecological determinants and adaptation. Journal of Field Ornithology, 87: 227-250. https://doi.org/10.1111/jofo.12157

Oro D. & Martínez-Abraín A. 2009. Ecology and behavior of seabirds. Marine Ecology, pp.364-389.

Ponchon A., Grémillet D., Doligez B., Chambert T., Tveera T., Gonzàles-Solìs J & Boulinier T. 2013. Tracking prospecting movements involved in breeding habitat selection: insights, pitfalls and perspectives. Methods in Ecology and Evolution, 4: 143-150. https://doi.org/10.1111/j.2041-210x.2012.00259.x

Thiebot J.-B., Delord K., Barbraud C., Marteau C. & Weimerskirch H. 2015. 167 individuals versus millions of hooks: bycatch mitigation in longline fisheries underlies conservation of Amsterdam albatrosses. Aquatic Conservation 26: 674-688. https://doi.org/10.1002/aqc.2578

Whitford M & Klimley A. P. An overview of behavioral, physiological, and environmental sensors used in animal biotelemetry and biologging studies. Animal Biotelemetry, 7: 26. https://doi.org/10.1186/s40317-019-0189-z

Wooller R.D., Bradley J. S. & Croxall J. P. 1992. Long-term population studies of seabirds. Trends in Ecology and Evolution, 7: 111-114. https://doi.org/10.1016/0169-5347(92)90143-y

Wunderle J. M. 1991. Age-specific foraging proficiency in birds. Current Ornithology, 8: 273-324.

The challenges of independence: ontogeny of at-sea behaviour in a long-lived seabirdKarine Delord, Henri Weimerskirch, Christophe Barbraud<p style="text-align: justify;">The transition to independent foraging represents an important developmental stage in the life cycle of most vertebrate animals. Juveniles differ from adults in various life history traits and tend to survive less w...Behaviour & Ethology, Foraging, OntogenyBlandine Doligez2021-10-26 07:51:49 View
14 Dec 2022
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The contrasted impacts of grasshoppers on soil microbial activities in function of primary production and herbivore diet

Complex interactions between ecosystem productivity and herbivore diets lead to non-predicted effects on nutrient cycling

Recommended by based on reviews by Manuel Blouin and Tord Ranheim Sveen

The authors present a study typical of the field of belowground-aboveground interactions [1]. This framework has been extremely fruitful since the beginning of 2000s [2]. It has also contributed to bridge the gap between soil ecology and the rest of ecology [3]. The study also pertains to the rich field on the impacts of herbivores on soil functioning [4].

The study more precisely tested during two years the effect on nutrient cycling of the interaction between the type of grassland (along a gradient of biomass productivity) and the diet of the community of insect herbivores (5 treatments manipulating the grasshopper community on 1 m2 plots, with a gradient from no grasshopper to grasshoppers either specialized on forbs or grasses). What seems extremely interesting is that the study is based on a rigorous hypothesis-testing approach. They compare the predictions of two frameworks: (1) The “productivity model” predicts that in productive ecosystems herbivores consume a high percentage of the net primary production thus accelerating nutrient cycling. (2) The “diet model” distinguishes herbivores consuming exploitative plants from those eating conservative plants. The former (later) type of herbivores favours conservative (exploitative) plants therefore decelerating (accelerating) nutrient cycling. Interestingly, the two frameworks have similar predictions (and symmetrically opposite predictions) in two cases out of four combinations between ecosystem productivities and types of diet (see Table 1). An other merit of the study is to combine in a rather comprehensive way all the necessary measurements to test these frameworks in combination: grasshopper diet, soil properties, characteristics of the soil microbial community, plant traits, vegetation survey and plant biomass.

The results were in contradiction with the ‘‘diet model’’: microbial properties and nitrogen cycling did not depend on grasshopper diet. The productivity of the grasslands did impact nutrient cycling but not in the direction predicted by the “productivity model”: productive grasslands hosted exploitative plants that depleted N resources in the soil and microbes producing few extracellular enzymes, which led to a lower potential N mineralization and a deceleration of nutrient cycling. Because, the authors stuck to their original hypotheses (that were not confirmed), they were able to discuss in a very relevant way their results and to propose some interpretations, at least partially based on the time scales involved by the productivity and diet models.

Beyond all the merits of this article, I think that two issues remain largely open in relation with the dynamics of the studied systems, and would deserve future research efforts. First, on the ‘‘short’’ term (up to several decades), can we predict how the communities of plants, soil microbes, and herbivores interact to drive the dynamics of the ecosystems? Second, at the evolutionary time scale, can we understand and predict the interactions between the evolution of plant, microbe and herbivore strategies and the consequences for the functioning of the grasslands? The two issues are difficult because of the multiple feedbacks involved. One way to go further would be to complement the empirical approach with models along existing research avenues [5, 6]. 

References

[1] Ibanez S, Foulquier A, Brun C, Colace M-P, Piton G, Bernard L, Gallet C, Clément J-C (2022) The contrasted impacts of grasshoppers on soil microbial activities in function of primary production and herbivore diet. bioRxiv, 2022.07.04.497718, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.07.04.497718

[2] Hooper, D. U., Bignell, D. E., Brown, V. K., Brussaard, L., Dangerfield, J. M., Wall, D. H., Wardle, D. A., Coleman, D. C., Giller, K. E., Lavelle, P., Van der Putten, W. H., De Ruiter, P. C., et al. 2000. Interactions between aboveground and belowground biodiversity in terretrial ecosystems: patterns, mechanisms, and feedbacks. BioScience, 50, 1049-1061. https://doi.org/10.1641/0006-3568(2000)050[1049:IBAABB]2.0.CO;2

[3] Barot, S., Blouin, M., Fontaine, S., Jouquet, P., Lata, J.-C., and Mathieu, J. 2007. A tale of four stories: soil ecology, theory, evolution and the publication system. PLoS ONE, 2, e1248. https://doi.org/10.1371/journal.pone.0001248

[4] Bardgett, R. D., and Wardle, D. A. 2003. Herbivore-mediated linkages between aboveground and belowground communities. Ecology, 84, 2258-2268. https://doi.org/10.1890/02-0274

[5] Barot, S., Bornhofen, S., Loeuille, N., Perveen, N., Shahzad, T., and Fontaine, S. 2014. Nutrient enrichment and local competition influence the evolution of plant mineralization strategy, a modelling approach. J. Ecol., 102, 357-366. https://doi.org/10.1111/1365-2745.12200

[6] Schweitzer, J. A., Juric, I., van de Voorde, T. F. J., Clay, K., van der Putten, W. H., Bailey, J. K., and Fox, C. 2014. Are there evolutionary consequences of plant-soil feedbacks along soil gradients? Func. Ecol., 28, 55-64. https://doi.org/10.1111/1365-2435.12201

 

The contrasted impacts of grasshoppers on soil microbial activities in function of primary production and herbivore dietSébastien Ibanez, Arnaud Foulquier, Charles Brun, Marie-Pascale Colace, Gabin Piton, Lionel Bernard, Christiane Gallet, Jean-Christophe Clément<p style="text-align: justify;">Herbivory can have contrasted impacts on soil microbes and nutrient cycling, which has stimulated the development of conceptual frameworks exploring the links between below- and aboveground processes. The "productiv...Ecosystem functioning, Herbivory, Soil ecology, Terrestrial ecologySébastien Barot2022-07-14 09:06:13 View
28 Sep 2020
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The dynamics of spawning acts by a semelparous fish and its associated energetic costs

Extreme weight loss: when accelerometer could reveal reproductive investment in a semelparous fish species

Recommended by ORCID_LOGO based on reviews by Aidan Jonathan Mark Hewison, Loïc Teulier and 1 anonymous reviewer

Continuous observation of animal behaviour could be quite a challenge in the field, and the situation becomes even more complicated with aquatic species mostly active at night. In such cases, biologging techniques are real game changers in ecology, behavioural ecology or eco-physiology. An accelerating number of methodological applications of these tools in natural condition are thus published each year [1]. Biologging is not limited to movement ecology. For instance, fine grain information about energy expenditure can be inferred from body acceleration [2], and accelerometers has already proven useful in monitoring reproductive costs in some fish species [3,4]. The first part of the study by Tentelier et al. [5] is in line with this growing literature. It describes measurements of energy expenditure during reproduction in a fish species, Allis shad (Alosa Alosa), based on tail beat frequency and occurrence of spawning acts. The study has been convincingly conducted, and the results are important for fish biologists. But this is not the whole story: the authors added to this otherwise classical study a very original and insightful analysis which deserves closer interest.
Tentelier et al. propose to use static accelerometer to monitor change in body roundness through the reproductive season. These semelparous fish first mature and built up reserves in the Atlantic Ocean and migrate into fresh water to reproduce. Contrary to iteroparous species, female shads do not have to strategically preserve energy for future reproduction. The females die few days after spawning having exhausted their energetic reserves: they typically lose almost half of their body mass during the spawning season. The beautiful idea in this study was to track down information about this dramatic slimming in the accelerometer data. Indeed, the accelerometer was attached on the side of the fish (close to the dorsal fin). A change in its angle with the vertical plane could be correlated with the change in roundness, the angle declining with the female thinning. Accelerometers have already been used to record body posture [6] but, in the present study, the novelty was to monitor the change in body shape.
Unfortunately, the data by Tentelier et al. are inconclusive so far. Broadly speaking, the accelerometer angle recorded declined through the spawning season, indicating an average slimming of the females, but there was no correlation between the change in angle and the mass loss at the individual level. This was partly due to the fact that the dorsal position of the accelerometer was not optimized to measures egg laying whose effects are mostly observable on ventral side.
Yet, this nice idea deserves more scrutiny. The method seems to be sensitive enough to detect inflation of swim bladder, the gas-filled organ helping the fish to control their position in the water column, as the accelerometer angle increased when the fish stayed close to the water surface. Additional works and proper calibration are certainly needed to validate the use of accelerometer angle as a proxy for body roundness. The actual data were not strong enough to justify a standalone publication on the subject, but it would have been shame to lose traces of such analysis and keep it in the file drawer. This is why I strongly support its report as a side question in a broader study. Science progresses not only with neat conclusive studies but also when unexpected (apparently anecdotal) observations stimulate new researches.

References

[1] Börger L, Bijleveld AI, Fayet AL, Machovsky‐Capuska GE, Patrick SC, Street GM and Vander Wal E. (2020) Biologging special feature. J. Anim. Ecol. 89, 6–15. 10.1111/1365-2656.13163
[2] Wilson RP et al. (2020) Estimates for energy expenditure in free‐living animals using acceleration proxies: A reappraisal. J. Anim. Ecol. 89, 161–172. 10.1111/1365-2656.13040
[3] Tsuda Y, Kawabe R, Tanaka H, Mitsunaga Y, Hiraishi T, Yamamoto K and Nashimoto K. (2006) Monitoring the spawning behaviour of chum salmon with an acceleration data logger. Ecol. Freshw. Fish 15, 264–274. 10.1111/j.1600-0633.2006.00147.x
[4] Sakaji H, Hamada K, Naito Y. 2018 Identifying spawning events of greater amberjack using accelerometers. Mar. Biol. Res. 14, 637–641. 10.1080/17451000.2018.1492140
[5] Tentelier C, Bouchard C, Bernardin A, Tauzin A, Aymes J-C, Lange F, Récapet C, Rives J (2020) The dynamics of spawning acts by a semelparous fish and its associated energetic costs. bioRxiv, 436295. doi: 10.1101/436295 ver. 7 peer-reviewed and recommended by PCI Ecology. 10.1101/436295
[6] Brown DD, Kays R, Wikelski M, Wilson R, Klimley AP. 2013 Observing the unwatchable through acceleration logging of animal behavior. Anim. Biotelemetry 1, 20. 10.1186/2050-3385-1-20

The dynamics of spawning acts by a semelparous fish and its associated energetic costsCédric Tentelier, Colin Bouchard, Anaïs Bernardin, Amandine Tauzin, Jean-Christophe Aymes, Frédéric Lange, Charlotte Recapet, Jacques Rives<p>1. During the reproductive season, animals have to manage both their energetic budget and gamete stock. In particular, for semelparous capital breeders with determinate fecundity and no parental care other than gametic investment, the depletion...Behaviour & Ethology, Freshwater ecology, Life historyFrancois-Xavier Dechaume-Moncharmont2020-06-04 15:18:56 View
02 Aug 2022
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The effect of dominance rank on female reproductive success in social mammals

When do dominant females have higher breeding success than subordinates? A meta-analysis across social mammals.

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

In this meta-analysis, Shivani et al. [1] investigate 1) whether dominance and reproductive success are generally associated across social mammals and 2) whether this relationship varies according to a) life history traits (e.g., stronger for species with large litter size), b) ecological conditions (e.g., stronger when resources are limited) and c) the social environment (e.g., stronger for cooperative breeders than for plural breeders). Generally, the results are consistent with their predictions, except there was no clear support for this relationship to be conditional on the ecological conditions. considered

As I have previously recommended the preregistration of this study [2,3], I do not have much to add here, as such recommendation should not depend on the outcome of the study. What I would like to recommend is the whole scientific process performed by the authors, from preregistration sent for peer review, to preprint submission and post-study peer review. It is particularly recommendable to notice that this project was a Masters student project, which shows that it is possible and worthy to preregister studies, even for such rather short-term projects. I strongly congratulate the authors for choosing this process even for an early career short-term project. I think it should be made possible for short-term students to conduct a preregistration study as a research project, without having to present post-study results. I hope this study can encourage a shift in the way we sometimes evaluate students’ projects.

I also recommend the readers to look into the whole pre- and post- study reviewing history of this manuscript and the associated preregistration, as it provides a better understanding of the process and a good example of the associated challenges and benefits [4]. It was a really enriching experience and I encourage others to submit and review preregistrations and registered reports!

 

References

[1] Shivani, Huchard, E., Lukas, D. (2022). The effect of dominance rank on female reproductive success in social mammals. EcoEvoRxiv, rc8na, ver. 10 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/osf.io/rc8na

[2] Shivani, Huchard, E., Lukas, D. (2020). Preregistration - The effect of dominance rank on female reproductive success in social mammals In principle acceptance by PCI Ecology of the version 1.2 on 07 July 2020. https://dieterlukas.github.io/Preregistration_MetaAnalysis_RankSuccess.html

[3] Paquet, M. (2020) Why are dominant females not always showing higher reproductive success? A preregistration of a meta-analysis on social mammals. Peer Community in Ecology, 100056. https://doi.org/10.24072/pci.ecology.100056

[4] Parker, T., Fraser, H., & Nakagawa, S. (2019). Making conservation science more reliable with preregistration and registered reports. Conservation Biology, 33(4), 747-750. https://doi.org/10.1111/cobi.13342

The effect of dominance rank on female reproductive success in social mammalsShivani, Elise Huchard, Dieter Lukas<p>Life in social groups, while potentially providing social benefits, inevitably leads to conflict among group members. In many social mammals, such conflicts lead to the formation of dominance hierarchies, where high-ranking individuals consiste...Behaviour & Ethology, Meta-analysesMatthieu Paquet2021-10-13 18:26:42 View
22 Apr 2021
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The hidden side of the Allee effect: correlated demographic traits and extinction risk in experimental populations

Allee effects under the magnifying glass

Recommended by ORCID_LOGO based on reviews by Tom Van Dooren, Dani Oro and 1 anonymous reviewer

For decades, the effect of population density on individual performance has been studied by ecologists using both theoretical, observational, and experimental approaches. The generally accepted definition of the Allee effect is a positive correlation between population density and average individual fitness that occurs at low population densities, while individual fitness is typically decreased through intraspecific competition for resources at high population densities.  Allee effects are very relevant in conservation biology because species at low population densities would then be subjected to much higher extinction risks. 

However, due to all kinds of stochasticity, low population numbers are always more vulnerable to extinction than larger population sizes. This effect by itself cannot be necessarily ascribed to lower individual performance at low densities, i.e, Allee effects. Vercken and colleagues (2021) address this challenging question and measure the extent to which average individual fitness is affected by population density analyzing 30 experimental populations. As a model system, they use populations of parasitoid wasps of the genus Trichogramma. They report Allee effect in 8 out 30 experimental populations. Vercken and colleagues's work has several strengths. 

First of all, it is nice to see that they put theory at work. This is a very productive way of using theory in ecology. As a starting point, they look at what simple theoretical population models say about Allee effects (Lewis and Kareiva 1993; Amarasekare 1998; Boukal and Berec 2002). These models invariably predict a one-humped relation between population-density and per-capita growth rate. It is important to remark that pure logistic growth, the paradigm of density-dependence, would never predict such qualitative behavior. It is only when there is a depression of per-capita growth rates at low densities that true Allee effects arise. Second, these authors manage to not only experimentally test this main prediction but also report additional demographic traits that are consistently affected by population density. 

In these wasps, individual performance can be measured in terms of the average number of individuals every adult is able to put into the next generation ---the lambda parameter in their analysis. The first panel in figure 3 shows that the per-capita growth rates are lower in populations presenting Allee effects, the ones showing a one-humped behavior in the relation between per-capita growth rates and population densities (see figure 2). Also other population traits, such maximum population size and exitinction probability, change in a correlated and consistent manner. 

In sum, Vercken and colleagues's results are experimentally solid and based on theory expectations. However, they are very intriguing. They find the signature of Allee effects in only 8 out 30 populations, all from the same genus Trichogramma, and some populations belonging to the same species (from different sampling sites) do not show consistently Allee effects. Where does this population variability comes from? What are the reasons underlying this within- and between-species variability? What are the individual mechanisms driving Allee effects in these populations? Good enough, this piece of work generates more intriguing questions than the question is able to clearly answer. Science is not a collection of final answers but instead good questions are the ones that make science progress. 

References

Amarasekare P (1998) Allee Effects in Metapopulation Dynamics. The American Naturalist, 152, 298–302. https://doi.org/10.1086/286169

Boukal DS, Berec L (2002) Single-species Models of the Allee Effect: Extinction Boundaries, Sex Ratios and Mate Encounters. Journal of Theoretical Biology, 218, 375–394. https://doi.org/10.1006/jtbi.2002.3084

Lewis MA, Kareiva P (1993) Allee Dynamics and the Spread of Invading Organisms. Theoretical Population Biology, 43, 141–158. https://doi.org/10.1006/tpbi.1993.1007

Vercken E, Groussier G, Lamy L, Mailleret L (2021) The hidden side of the Allee effect: correlated demographic traits and extinction risk in experimental populations. HAL, hal-02570868, ver. 4 peer-reviewed and recommended by Peer community in Ecology. https://hal.archives-ouvertes.fr/hal-02570868

The hidden side of the Allee effect: correlated demographic traits and extinction risk in experimental populationsVercken Elodie, Groussier Géraldine, Lamy Laurent, Mailleret Ludovic<p style="text-align: justify;">Because Allee effects (i.e., the presence of positive density-dependence at low population size or density) have major impacts on the dynamics of small populations, they are routinely included in demographic models ...Demography, Experimental ecology, Population ecologyDavid Alonso2020-09-30 16:38:29 View
01 Apr 2019
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The inherent multidimensionality of temporal variability: How common and rare species shape stability patterns

Diversity-Stability and the Structure of Perturbations

Recommended by ORCID_LOGO and based on reviews by Frederic Barraquand and 1 anonymous reviewer

In his 1972 paper “Will a Large Complex System Be Stable?” [1], May challenges the idea that large communities are more stable than small ones. This was the beginning of a fundamental debate that still structures an entire research area in ecology: the diversity-stability debate [2]. The most salient strength of May’s work was to use a mathematical argument to refute an idea based on the observations that simple communities are less stable than large ones. Using the formalism of dynamical systems and a major results on the distribution of the eigen values for random matrices, May demonstrated that the addition of random interactions destabilizes ecological communities and thus, rich communities with a higher number of interactions should be less stable. But May also noted that his mathematical argument holds true only if ecological interactions are randomly distributed and thus concluded that this must not be true! This is how the contradiction between mathematics and empirical observations led to new developments in the study of ecological networks.
Since 1972, the theoretical corpus of ecology has advanced, building on the formalism of dynamical systems, ecologists have revealed that ecological interactions are indeed not randomly distributed [3,4], but general rules are still missing and we are far from understanding what determine the exact network topology of a given community. One promising avenue is to understand the relationship between different facets of the concept of stability [5,6]. Indeed, the classical approach to determine whether a system is stable is qualitative: if a system returns to its equilibrium when it is slightly moved away from it, then the system is considered stable. But there are several other aspects that are worth scrutinizing. For instance, when a system returns to its equilibrium, one can characterize the corresponding transient dynamics [7,8], that is asking fundamental questions such as: what is the trajectory of return? How long does it take to return to the equilibrium? Another fundamental question is whether the system remains qualitatively stable when the distributions of interactions strengths change? From a biological standpoint, all of these questions matter as all these aspects of stability may partially explain the actual structure of ecological networks, and hence, frameworks that integrate several facets of stability are much needed.
The study by Arnoldi et al. [9] is a significant step towards such a framework. The strength of their formalism is threefold. First, instead of considering separately the system and its perturbations, they considering the fluctuations of a perturbed ecological systems and thus, perturbations are parts of the ecological system. Second, they use of a broad definition of perturbation that encompasses the types of perturbations (whether the individual respond synchronously or not), their intensity and their direction (how the perturbations are correlated across species). Third, they quantify the instability of the system using variability which integrates the consequences of perturbations over the whole set of species of a community: such a measure is comparable across communities and accounts for the trivial effect of the perturbations on the system dynamics.
Using this framework, the authors show that interactions within a stable community leads to a general relationship between variability and the abundance of individually perturbed species: if individuals of species respond in synchrony to a perturbation, then the more abundant the species perturbed the higher the variability of the system, but the relationship is reverse when individual respond asynchronously. A direct implications of these results for the classical debate is that the diversity-stability relationship is negative for the former type of perturbations (as in May’s seminal paper) but positive for the latter type. Hence, the rigorous work of Arnoldi and colleagues sheds a new light upon the classical debate: the nature of the perturbation regime prevailing within a community affects the slope of the diversity-stability relationships and given the vast diversity of ecological communities, this may very well be one of the reasons why the debate still endures.
From a historical perspective, it is interesting that ecologists have gone from looking at random webs to structured webs and now, in a sense, Arnoldi et al. are unpacking the role of differentially structured perturbations. The work they achieved will doubtlessly be followed by further theoretical investigations. One natural research avenue is to revisit the role of the topology of ecological networks with this framework: how the distribution of interactions and their strength affect the general relationship they unravel? Finally, this study demonstrate that the impact of the abundance of a species on the variability of the system depends on the nature of the perturbation regime and so the distribution of species abundances within a community should be determined by the prevailing perturbation regime which is a prediction that remains to be tested.

References

[1] May, Robert M (1972). Will a Large Complex System Be Stable? Nature 238, 413–414. doi: 10.1038/238413a0
[2] McCann, Kevin Shear (2000). The Diversity–Stability Debate. Nature 405, 228–233. doi: 10.1038/35012234
[3] Rooney, Neil, Kevin McCann, Gabriel Gellner, and John C. Moore (2006). Structural Asymmetry and the Stability of Diverse Food Webs. Nature 442, 265–269. doi: 10.1038/nature04887
[4] Jacquet, Claire, Charlotte Moritz, Lyne Morissette, Pierre Legagneux, François Massol, Philippe Archambault, and Dominique Gravel (2016). No Complexity–Stability Relationship in Empirical Ecosystems. Nature Communications 7, 12573. doi: 10.1038/ncomms12573
[5] Donohue, Ian, Helmut Hillebrand, José M. Montoya, Owen L. Petchey, Stuart L. Pimm, Mike S. Fowler, Kevin Healy, et al. (2016). Navigating the Complexity of Ecological Stability. Ecology Letters 19, 1172–1185. doi: 10.1111/ele.12648
[6] Arnoldi, Jean-François, and Bart Haegeman (2016). Unifying Dynamical and Structural Stability of Equilibria. Proceedings of the Royal Society A: Mathematical, Physical and Engineering Science 472, 20150874. doi: 10.1098/rspa.2015.0874
[7] Caswell, Hal, and Michael G. Neubert (2005). Reactivity and Transient Dynamics of Discrete-Time Ecological Systems. Journal of Difference Equations and Applications 11, 295–310. doi: 10.1080/10236190412331335382
[8] Arnoldi, J-F., M. Loreau, and B. Haegeman (2016). Resilience, Reactivity and Variability: A Mathematical Comparison of Ecological Stability Measures. Journal of Theoretical Biology 389, 47–59. doi: 10.1016/j.jtbi.2015.10.012
[9] Arnoldi, Jean-Francois, Michel Loreau, and Bart Haegeman. (2019). The Inherent Multidimensionality of Temporal Variability: How Common and Rare Species Shape Stability Patterns.” BioRxiv, 431296, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/431296

The inherent multidimensionality of temporal variability: How common and rare species shape stability patternsJean-François Arnoldi, Michel Loreau, Bart Haegeman<p>Empirical knowledge of ecosystem stability and diversity-stability relationships is mostly based on the analysis of temporal variability of population and ecosystem properties. Variability, however, often depends on external factors that act as...Biodiversity, Coexistence, Community ecology, Competition, Interaction networks, Theoretical ecologyKevin Cazelles2018-10-02 14:01:03 View
18 Apr 2024
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The large and central Caligo martia eyespot may reduce fatal attacks by birds: a case study supports the deflection hypothesis in nature

Intimidation or deflection: field experiments in a tropical forest to simultaneously test two competing hypotheses about how butterfly eyespots confer protection against predators

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Eyespots—round or oval spots, usually accompanied by one or more concentric rings, that together imitate vertebrate eyes—are found in insects of at least three orders and in some tropical fishes (Stevens 2005). They are particularly frequent in Lepidoptera, where they occur on wings of adults in many species (Monteiro et al. 2006), and in caterpillars of many others (Janzen et al. 2010). The resemblance of eyespots to vertebrate eyes often extends to details, such as fake « pupils » (round or slit-like) and « eye sparkle » (Blut et al. 2012). Larvae of one hawkmoth species even have fake eyes that appear to blink (Hossie et al. 2013). Eyespots have interested evolutionary biologists for well over a century. While they appear to play a role in mate choice in some adult Lepidoptera, their adaptive significance in adult Lepidoptera, as in caterpillars, is mainly as an anti-predator defense (Monteiro 2015). However, there are two competing hypotheses about the mechanism by which eyespots confer defense against predators. The « intimidation » hypothesis postulates that eyespots intimidate potential predators, startling them and reducing the probability of attack. The « deflection » hypothesis holds that eyespots deflect attacks to parts of the body where attack has relatively little effect on the animal’s functioning and survival. In caterpillars, there is little scope for the deflection hypothesis, because attack on any part of a caterpillar’s body is likely to be lethal. Much observational and some experimental evidence supports the intimidation hypothesis in caterpillars (Hossie & Sherratt 2012). In adult Lepidoptera, however, both mechanisms are plausible, and both have found support (Stevens 2005). The most spectacular examples of intimidation are in butterflies in which eyespots located centrally in hindwings and hidden in the natural resting position are suddenly exposed, startling the potential predator (e.g., Vallin et al. 2005). The most spectacular examples of deflection are seen in butterflies in which eyespots near the hindwing margin combined with other traits give the appearance of a false head (e.g., Chotard et al. 2022; Kodandaramaiah 2011). 

Most studies have attempted to test for only one or the other of these mechanisms—usually the one that seems a priori more likely for the butterfly species being studied. But for many species, particularly those that have neither spectacular startle displays nor spectacular false heads, evidence for or against the two hypotheses is contradictory.  

Iserhard et al. (2024) attempted to simultaneously test both hypotheses, using the neotropical nymphalid butterfly Caligo martia. This species has a large ventral hindwing eyespot, exposed in the insect’s natural resting position, while the rest of the ventral hindwing surface is cryptically coloured. In a previous study of this species, De Bona et al. (2015) presented models with intact and disfigured eyespots on a computer monitor to a European bird species, the great tit (Parus major). The results favoured the intimidation hypothesis. Iserhard et al. (2024) devised experiments presenting more natural conditions, using fairly realistic dummy butterflies, with eyespots manipulated or unmanipulated, exposed to a diverse assemblage of insectivorous birds in nature, in a tropical forest. Using color-printed paper facsimiles of wings, with eyespots present, UV-enhanced, or absent, they compared the frequency of beakmarks on modeling clay applied to wing margins (frequent attacks would support the deflection hypothesis) and (in one of two experiments) on dummies with a modeling-clay body (eyespots should lead to reduced frequency of attack, to wings and body, if birds are intimidated). Their experiments also included dummies without eyespots whose wings were either cryptically coloured (as in unmanipulated butterflies) or not. Their results, although complex, indicate support for the deflection hypothesis: dummies with eyespots were mostly attacked on these less vital parts. Dummies lacking eyespots were less frequently attacked, especially when they were camouflaged. Camouflaged dummies without eyespots were in fact the least frequently attacked of all the models. However, when dummies lacking eyespots were attacked, attacks were usually directed to vital body parts. These results show some of the complexity of estimating costs and benefits of protective conspicuous signals vs. camouflage (Stevens et al. 2008).

Two complementary experiments were conducted. The first used facsimiles with « wings » in a natural resting position (folded, ventral surfaces exposed), but without a modeling-clay « body ». In the second experiment, facsimiles had a modeling-clay « body », placed between the two unfolded wings to make it as accessible to birds as the wings. However, these dummies displayed the ventral surfaces of unfolded wings, an unnatural resting position. The study was thus not able to compare bird attacks to the body vs. wings in a natural resting position. One can understand the reason for this methodological choice, but it is a limitation of the study.

The naturalness of the conditions under which these field experiments were conducted is a strong argument for the biological significance of their results. However, the uncontrolled conditions naturally result in many questions being left open. The butterfly dummies were exposed to at least nine insectivorous bird species. Do bird species differ in their behavioral response to eyespots? Do responses depend on the distance at which a bird first detects the butterfly? Do eyespots and camouflage markings present on the same animal both function, but at different distances (Tullberg et al. 2005)? Do bird responses vary depending on the particular light environment in the places and at the times when they encounter the butterfly (Kodandaramaiah 2011)? Answering these questions under natural, uncontrolled conditions will be challenging, requiring onerous methods, (e.g., video recording in multiple locations over time). The study indicates the interest of pursuing these questions.

References

Blut, C., Wilbrandt, J., Fels, D., Girgel, E.I., & Lunau, K. (2012). The ‘sparkle’ in fake eyes–the protective effect of mimic eyespots in Lepidoptera. Entomologia Experimentalis et Applicata, 143, 231-244. https://doi.org/10.1111/j.1570-7458.2012.01260.x

Chotard, A., Ledamoisel, J., Decamps, T., Herrel, A., Chaine, A.S., Llaurens, V., & Debat, V. (2022). Evidence of attack deflection suggests adaptive evolution of wing tails in butterflies. Proceedings of the Royal Society B, 289, 20220562. https://doi.org/10.1098/rspb.2022.0562

De Bona, S., Valkonen, J.K., López-Sepulcre, A., & Mappes, J. (2015). Predator mimicry, not conspicuousness, explains the efficacy of butterfly eyespots. Proceedings of the Royal Society B, 282, 1806. https://doi.org/10.1098/RSPB.2015.0202

Hossie, T.J., & Sherratt, T.N. (2012). Eyespots interact with body colour to protect caterpillar-like prey from avian predators. Animal Behaviour, 84, 167-173. https://doi.org/10.1016/j.anbehav.2012.04.027

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The large and central *Caligo martia* eyespot may reduce fatal attacks by birds: a case study supports the deflection hypothesis in natureCristiano Agra Iserhard, Shimene Torve Malta, Carla Maria Penz, Brenda Barbon Fraga, Camila Abel da Costa, Taiane Schwantz, Kauane Maiara Bordin<p>Many animals have colorations that resemble eyes, but the functions of such eyespots are debated. Caligo martia (Godart, 1824) butterflies have large ventral hind wing eyespots, and we aimed to test whether these eyespots act to deflect or to t...Biodiversity, Community ecology, Conservation biology, Life history, Tropical ecologyDoyle Mc Key2023-11-21 15:00:20 View