In temperate regions, food abundance and quality vary greatly throughout the year, and the ability of organisms to synchronise their phenology to these changes is a key determinant of their reproductive success. Successful synchronisation requires that cues are perceived prior to change, leaving time for physiological adjustments.
But what are the cues used to anticipate seasonal changes? Abiotic factors like temperature and photoperiod are known for their driving role in the phenology of a wide range of plant an animal species [1,2] . Arguably though, biotic cues directly linked to upcoming changes in food abundance could be as important as abiotic factors, but the response of organisms to these cues remains relatively unexplored.
Biotic cues may be particularly important for higher trophic levels because of their tight interaction with the hosts or preys they depend on. In this study Tougeron and colleagues [3] address this topic using interacting insects, namely herbivorous aphids and the parasitic wasps (or parasitoids) that feed on them. The key finding of the study by Tougeron et al. [3] is that the host morph in which parasitic wasp larvae develop is a major driver of diapause induction. More importantly, the aphid morph that triggers diapause in the wasp is the one that will lay overwintering eggs in autumn at the onset of harsh winter conditions. Its neatly designed experimental setup also provides evidence that this response may vary across populations as host-dependent diapause induction was only observed in a wasp population that originated from a cold area. As the authors suggests, this may be caused by local adaptation to environmental conditions because, relative to warmer regions, missing the time window to enter diapause in colder regions may have more dramatic consequences. The study also shows that different aphid morphs differ greatly in their chemical composition, and points to particular types of metabolites like sugars and polyols as specific cues for diapause induction.
This study provides a nice example of the complexity of biological interactions, and of the importance of phenological synchrony between parasites and their hosts. The authors provide evidence that phenological synchrony is likely to be achieved via chemical cues derived from the host. A similar approach was used to demonstrate that the herbivorous beetle Leptinotarsa decemlineata uses plant chemical cues to enter diapause [4]. Beetles fed on plants exposed to pre-wintering conditions entered diapause in higher proportions than those fed on control plants grown at normal conditions. As done by Tougeron et al. [3], in [4] the authors associated diapause induction to changes in the composition of metabolites in the plant. In both studies, however, the missing piece is to unveil the particular chemical involved, an answer that may be provided by future experiments.
Latitudinal clines in diapause induction have been described in a number of insect species [5]. Correlative studies, in which the phenology of different trophic levels has been monitored, suggest that these clines may in part be governed by lower trophic levels. For example, Phillimore et al. [6] explored the relative contribution of temperature and of host plant phenology on adult flight periods of the butterfly Anthocharis cardamines. Tougeron et al. [3], by using aphids and their associated parasitoids, take the field further by moving from observational studies to experiments. Besides, aphids are not only a tractable host-parasite system in the laboratory, they are important agricultural pests. Improving our basic knowledge of their ecological interactions may ultimately contribute to improving pest control techniques. The study by Tougeron et al. [3] exemplifies the multiple benefits that can be gained from addressing fundamental questions in species that are also directly relevant to society.

References

[1] Tauber, M. J., Tauber, C. A., and Masaki, S. (1986). Seasonal Adaptations of Insects. Oxford, New York: Oxford University Press.
[2] Bradshaw, W. E., and Holzapfel, C. M. (2007). Evolution of Animal Photoperiodism. Annual Review of Ecology, Evolution, and Systematics, 38(1), 1–25. doi: 10.1146/annurev.ecolsys.37.091305.110115
[3] Tougeron, K., Brodeur, J., Baaren, J. van, Renault, D., and Lann, C. L. (2019b). Sex makes them sleepy: host reproductive status induces diapause in a parasitoid population experiencing harsh winters. bioRxiv, 371385, ver. 6 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/371385
[4] Izzo, V. M., Armstrong, J., Hawthorne, D., and Chen, Y. (2014). Time of the season: the effect of host photoperiodism on diapause induction in an insect herbivore, Leptinotarsa decemlineata. Ecological Entomology, 39(1), 75–82. doi: 10.1111/een.12066
[5] Hut Roelof A., Paolucci Silvia, Dor Roi, Kyriacou Charalambos P., and Daan Serge. (2013). Latitudinal clines: an evolutionary view on biological rhythms. Proceedings of the Royal Society B: Biological Sciences, 280(1765), 20130433. doi: 10.1098/rspb.2013.0433
[6] Phillimore, A. B., Stålhandske, S., Smithers, R. J., and Bernard, R. (2012). Dissecting the Contributions of Plasticity and Local Adaptation to the Phenology of a Butterfly and Its Host Plants. The American Naturalist, 180(5), 655–670. doi: 10.1086/667893

Across the temporal expanse of history, the impact of human activities on global landscapes has manifested as a complex interplay of ecological alterations. From the advent of early agricultural practices to the successive waves of industrialization characterizing the 18th and 19th centuries, anthropogenic forces have exerted profound and enduring transformations upon Earth's ecosystems. Indeed, by 2017, more than 80% of the terrestrial biosphere was transformed by human populations and land use, and just 19% remains as wildlands (Ellis et al. 2021).
 
Urbanization engenders profound alterations in environmental conditions, exerting substantial impacts on biological communities. The expansion of built infrastructure, modification of land use patterns, and the introduction of impervious surfaces and habitat fragmentation are key facets of urbanization (Faeth et al. 2011). These alterations generate biodiversity loss, changes in the composition of biological communities, disruptions in access and availability of food and nutrients, and a loss of efficiency in the immune system's control of infections, etc. (Reyes et al. 2013).
 
In this study, Caizergues et al. (2023) investigated the prevalence and diversity of avian malaria parasites (Plasmodium/Haemoproteus sp. and Leucocytozoon sp.) in great tits (Parus major) living across an urbanization gradient. The study reveals nuanced patterns of avian malaria prevalence and lineage diversity in great tits across urban and non-urban environments. While overall parasite diversity remains consistent, there are marked differences in prevalence between life stages and habitats. They observed a high prevalence in adult birds (from 95% to 100%), yet lower prevalence in fledglings (from 0% to 38%). Notably, urban nestlings exhibit higher parasite prevalence than their non-urban counterparts, suggesting a potential link between early malaria infection and the urban heat island effect. This finding underscores the importance of considering both spatial and temporal aspects of urbanization in understanding disease dynamics. Parasite lineages were not habitat-specific. The results suggest a potential parasitic burden in more urbanized areas, with a marginal but notable effect of nest-level urbanization on Plasmodium prevalence. This challenges the common perception of lower parasitic prevalence in urban environments and highlights the need for further investigation into the factors influencing parasite prevalence at finer spatial scales.
 
The discussion emphasizes the significance of examining vector distributions, abundance, and diversity in urban areas, which may be influenced by ecological niches and the presence of suitable habitats such as marshes. The identification of habitat-specific Haemosporidian lineages, particularly those occurring more frequently in urban areas, raises intriguing questions about the factors influencing parasite diversity. The presence of rare lineages in urban environments, such as AFR065, DELURB4, and YWT4, suggests a potential connection between urban bird communities and specific parasite strains.
 
Future research should empirically demonstrate these relationships to enhance our understanding of urban parasitology. This finding has broader implications for wildlife epidemiology, especially when introducing or keeping exotic wildlife in contact with native species. The study highlights the importance of considering not only the prevalence but also the specific lineages of parasites in understanding the dynamics of avian malaria in urban and non-urban habitats. This preprint contributes valuable insights to the ongoing discourse on the intricate interplay between ecological repercussions of human-induced changes (urbanization), biological communities, and the prevalence of vector-borne diseases.
 
References

Caizergues AE, Robira B, Perrier C, Jeanneau M, Berthomieu A, Perret S, Gandon S, Charmantier A (2023) Cities as parasitic amplifiers? Malaria prevalence and diversity in great tits along an urbanization gradient. bioRxiv, 2023.05.03.539263, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2023.05.03.539263

Ellis EC, Gauthier N, Klein Goldewijk K, Bliege Bird R, Boivin N, Díaz S, Fuller DQ, Gill JL, Kaplan JO, Kingston N, Locke H, McMichael CNH, Ranco D, Rick TC, Shaw MR, Stephens L, Svenning JC, Watson JEM. People have shaped most of terrestrial nature for at least 12,000 years. Proc Natl Acad Sci U S A. 2021 Apr 27;118(17):e2023483118. https://doi.org/10.1073/pnas.2023483118. 

Faeth  SH, Bang  C, Saari  S (2011) Urban biodiversity: Patterns and mechanisms. Ann N Y Acad Sci 1223:69–81. https://doi.org/10.1111/j.1749-6632.2010.05925.x

Faeth  SH, Bang  C, Saari  S (2011) Urban biodiversity: Patterns and mechanisms. Ann N Y Acad Sci 1223:69–81. https://doi.org/10.1111/j.1749-6632.2010.05925.x

Reyes  R, Ahn  R, Thurber  K, Burke  TF (2013) Urbanization and Infectious Diseases: General Principles, Historical Perspectives, and Contemporary Challenges. Challenges Infect Dis 123. https://doi.org/10.1007/978-1-4614-4496-1_4

Temperature-size rule (TSR) is a phenomenon of plastic changes in body size in response to temperature, originally observed in more than 80% of ectothermic organisms representing various groups (Atkinson 1994). In particular, ectotherms were observed to grow faster and reach smaller size at higher temperature and grow slower and achieve larger size at lower temperature. This response has fired the imagination of researchers since its invention, due to its counterintuitive pattern from an evolutionary perspective (Berrigan and Charnov 1994). The main question to be resolved is: why do organisms grow fast and achieve smaller sizes under more favourable conditions (= relatively higher temperature), while they grow longer and achieve larger sizes under less favourable conditions (relatively lower temperature), if larger size means higher fitness, while longer development may be risky? 

This evolutionary conundrum still awaits an ultimate explanation (Angilletta Jr et al. 2004; Angilletta and Dunham 2003; Verberk et al. 2021). Although theoretical modelling has shown that such a growth pattern can be achieved as a response to temperature alone, with a specific combination of energetic parameters and external mortality (Kozłowski et al. 2004), it has been suggested that other temperature-dependent environmental variables may be the actual drivers of this pattern. One of the most frequently invoked variable is the relative oxygen availability in the environment (e.g., Atkinson et al. 2006; Audzijonyte et al. 2019; Verberk et al. 2021; Woods 1999), which decreases with temperature increase. Importantly, this effect is more pronounced in aquatic systems (Forster et al. 2012). However, other temperature-dependent parameters are also being examined in the context of their possible effect on TSR induction and strength.

Food availability is among the interfering factors in this regard. In aquatic systems, nutritional conditions are generally better at higher temperature, while a range of relatively mild thermal conditions is considered. However, there are no conclusive results so far on how nutritional conditions affect the plastic body size response to acute temperature changes. A study by Bazin et al. (2023) examined this particular issue, the effects of food and temperature on TSR, in medaka fish. An important value of the study was to relate the patterns found to fitness. This is a rare and highly desirable approach since evolutionary significance of any results cannot be reliably interpreted unless shown as expressed in light of fitness. 

The authors compared the body size of fish kept at 20°C and 30°C under conditions of food abundance or food restriction. The results showed that the TSR (smaller body size at 30°C compared to 20°C) was observed in both food treatments, but the effect was delayed during fish development under food restriction. Regarding the relevance to fitness, increased temperature resulted in more eggs laid but higher mortality, while food restriction increased survival but decreased the number of eggs laid in both thermal treatments. Overall, food restriction seemed to have a more severe effect on development at 20°C than at 30°C, contrary to the authors’ expectations. 

I found this result particularly interesting. One possible interpretation, also suggested by the authors, is that the relative oxygen availability, which was not controlled for in this study, could have affected this pattern. According to theoretical predictions confirmed in quite many empirical studies so far, oxygen restriction is more severe at higher temperatures. Perhaps for these particular two thermal treatments and in the case of the particular species studied, this restriction was more severe for organismal performance than the food restriction. This result is an example that all three variables, temperature, food and oxygen, should be taken into account in future studies if the interrelationship between them is to be understood in the context of TSR. It also shows that the reasons for growing smaller in warm may be different from those for growing larger in cold, as suggested, directly or indirectly, in some previous studies (Hessen et al. 2010; Leiva et al. 2019). 

Since medaka fish represent predatory vertebrates, the results of the study contribute to the issue of global warming effect on food webs, as the authors rightly point out. This is an important issue because the general decrease in the size or organisms in the aquatic environment with global warming is a fact (e.g., Daufresne et al. 2009), while the question of how this might affect entire communities is not trivial to resolve (Ohlberger 2013). 

REFERENCES

Angilletta Jr, M. J., T. D. Steury & M. W. Sears, 2004. Temperature, growth rate, and body size in ectotherms: fitting pieces of a life–history puzzle. Integrative and Comparative Biology 44:498-509. https://doi.org/10.1093/icb/44.6.498

Angilletta, M. J. & A. E. Dunham, 2003. The temperature-size rule in ectotherms: Simple evolutionary explanations may not be general. American Naturalist 162(3):332-342. https://doi.org/10.1086/377187

Atkinson, D., 1994. Temperature and organism size – a biological law for ectotherms. Advances in Ecological Research 25:1-58. https://doi.org/10.1016/S0065-2504(08)60212-3

Atkinson, D., S. A. Morley & R. N. Hughes, 2006. From cells to colonies: at what levels of body organization does the 'temperature-size rule' apply? Evolution & Development 8(2):202-214 https://doi.org/10.1111/j.1525-142X.2006.00090.x

Audzijonyte, A., D. R. Barneche, A. R. Baudron, J. Belmaker, T. D. Clark, C. T. Marshall, J. R. Morrongiello & I. van Rijn, 2019. Is oxygen limitation in warming waters a valid mechanism to explain decreased body sizes in aquatic ectotherms? Global Ecology and Biogeography 28(2):64-77 https://doi.org/10.1111/geb.12847

Bazin, S., Hemmer-Brepson, C., Logez, M., Sentis, A. & Daufresne, M. 2023. Distinct impacts of food restriction and warming on life history traits affect population fitness in vertebrate ectotherms. HAL, ver.3  peer-reviewed and recommended by PCI Ecology. https://hal.inrae.fr/hal-03738584v3

Berrigan, D. & E. L. Charnov, 1994. Reaction norms for age and size at maturity in response to temperature – a puzzle for life historians. Oikos 70:474-478. https://doi.org/10.2307/3545787

Daufresne, M., K. Lengfellner & U. Sommer, 2009. Global warming benefits the small in aquatic ecosystems. Proceedings of the National Academy of Sciences USA 106(31):12788-93 https://doi.org/10.1073/pnas.0902080106

Forster, J., A. G. Hirst & D. Atkinson, 2012. Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proceedings of the National Academy of Sciences of the United States of America 109(47):19310-19314. https://doi.org/10.1073/pnas.1210460109

Hessen, D. O., P. D. Jeyasingh, M. Neiman & L. J. Weider, 2010. Genome streamlining and the elemental costs of growth. Trends in Ecology & Evolution 25(2):75-80. https://doi.org/10.1016/j.tree.2009.08.004

Kozłowski, J., M. Czarnoleski & M. Dańko, 2004. Can optimal resource allocation models explain why ectotherms grow larger in cold? Integrative and Comparative Biology 44(6):480-493. https://doi.org/10.1093/icb/44.6.480

Leiva, F. P., P. Calosi & W. C. E. P. Verberk, 2019. Scaling of thermal tolerance with body mass and genome size in ectotherms: a comparison between water- and air-breathers. Philosophical Transactions of the Royal Society B 374:20190035. https://doi.org/10.1098/rstb.2019.0035

Ohlberger, J., 2013. Climate warming and ectotherm body szie - from individual physiology to community ecology. Functional Ecology 27:991-1001. https://doi.org/10.1111/1365-2435.12098

Verberk, W. C. E. P., D. Atkinson, K. N. Hoefnagel, A. G. Hirst, C. R. Horne & H. Siepel, 2021. Shrinking body sizes in response to warming: explanations for the temperature-size rule with special emphasis on the role of oxygen. Biological Reviews 96:247-268. https://doi.org/10.1111/brv.12653

Woods, H. A., 1999. Egg-mass size and cell size: effects of temperature on oxygen distribution. American Zoologist 39:244-252. https://doi.org/10.1093/icb/39.2.244

As mankind develops increasingly efficient and productive methods of agriculture and food production, we have reached a point where intensive agriculture threatens several aspects of life on Earth, negatively affecting biodiversity, carbon, nitrogen and phosphorus cycles and water reservoirs, while producing considerable amounts of greenhouse gases (Krebs and Bach, 2018). There was a need to develop farming methods that were friendly to both nature and people, producing good quality, healthy food without destroying the environment. The idea of permaculture, a concept of sustainable agriculture based on methods learned directly from nature, originated in the 1960s, invented and developed by Bruce Charles Mollison and David Holmgren (Mollison and Holmgren 1979, Mollison et al. 1991, Holmgren 2002). Although the idea of permaculture has attracted scientific interest, the representation in published studies is unbalanced in favour of positive ecological and sociological effects, with much less presence of rigorous experimental testing (Ferguson and Lovell 2014, Reiff et al. 2024a).

Reiff et al. (2024b) provided the first large-scale empirical evidence of permaculture production outcomes for Central Europe. Based on results from 11 commercial permaculture sites, situated mostly in Germany but also in Switzerland and Luxembourg, the authors found that food production from permaculture sites was on average comparable to that from conventional and organic agriculture. The authors were very thorough in pointing out the issues that could potentially affect their results and which need further testing.

Among these, the authors highlight the considerable variability between the 11 sites studied, which may suggest that different permacultures should differ in details according to their specificity - an interesting issue that definitely requires further study. The other factor that the authors point out that could have influenced the results and led to an underestimation of the real potential is the age of the permaculture sites. The sites from the study were relatively young, and their potential can be expected to increase with time.

It is important to note that the results are mostly applicable to vegetables, as vegetable production accounted for 94% of production in the permaculture sites (followed by tree crops, 6%, and soft fruit production, 0.5%). There is therefore a need to include other types of crops produced in further studies of this type.

To date, the results informing permaculture food production are urgently needed and should cover the potentially wide range of geographical regions and crops produced. The results of Reiff et al. (2025) show that rigorous testing of this issue is demanding, but the authors provide a very sound "road map" of further steps.      

Literature:

Ferguson R. S. and Lovell S. T. 2014. Permaculture for agroecology: design, movement, practice, and worldview. A review. Agronomy for Sustainable Development 34, 251-274. https://doi.org/10.1007/s13593-013-0181-6

Holmgren D. 2002. Permaculture: Principles & Pathways Beyond Sustainability. Holmgren Design Services, pp. 320.

Krebs J. and Bach S. 2018. Permaculture – scientific evidence of principles for the agroecological design of farming systems. Sustainability 10, 3218, https://doi.org/10.3390/su10093218

Mollison B. C. and Holmgren D. 1979. Permaculture One: A Perennial Agricultural System for Human Settlements. Tagari Publications, pp. 136.

Mollison B. C., Slay, R. M. and Jeeves A. 1991. Introduction to permaculture. Tagari Publications, pp. 198.

Reiff J., Jungkunst H. F., Mauser K. M., Kampel S., Regending S., Rösch V., Zaller J. G. and Entling M. H. 2024a. Permaculture enhances carbon stocks, soil quality and biodiversity in Central Europe. Communications Earth & Environment 5, 305. https://doi.org/10.1038/s43247-024-01405-8

Reiff J., Jungkunst H. F., Antes N. and Entling M. H. 2024b. Crop productivity of Central European Permaculture is within the range of organic and conventional agriculture. bioRxiv, ver.2 peer-reviewed and recommended by PCI Ecology. https://doi.org/10.1101/2024.09.09.611985

In their pre-registered paper [1], McCune and colleagues propose a field-based study of social versus individual learning mechanisms in an avian species (great-tailed grackles) that has been expanding its geographic range. The study forms part of a longer-term project that addresses various aspects of this species’ behaviour and biology, and the experience of the team is clear from the preprint. Assessing variation in learning mechanisms in different sections of the grackles’ distribution range, the researchers will investigate how individual learning and social transmission may impact learning about novel challenges in the environment. Considering that this is a social species, the authors expect both individual learning and social transmission to occur, when groups of grackles encounter new challenges/ opportunities in the wild. This in itself is not a very unusual idea to test [2, 3], but the authors are rigorously distinguishing between imitation, emulation, local enhancement, and social enhancement. Such rigour is certainly valuable in studies of cognition in the wild.
Further, the authors predict that the contribution of individual versus social learning could vary between populations, as the core may contain fewer unfamiliar/novel stimuli than the edge, where artificial sources of water (for example) may be more common. They make an argument that the core, middle, and edge populations would experience differing levels of environmental predictability. If true, their field experiments could yield very novel results on how changes in environmental predictability affect social/individual learning in a single study species. Their data would then give unusual insights into the ecological value of individual learning and distinct forms of social learning – something that is not easy to test in wild animals. The authors consider a variety of alternative hypotheses that may ultimately explain their findings, and clarify their methods and analyses in fine detail. The authors also set out limitations clearly, and give a thorough account of their approaches and thinking.
The reviewers and I have a still-unanswered question, which is central to the study: what is the predictability or unpredictability of the core versus edge environments? Although the authors have explained similarities and distinctions between the different sections of the grackles’ range, their description feels a bit vague -- it's not as rigorous or well-defined as the rest of the paper. Such a lack of definition may be inevitable in the limitations of a preprint, but ultimately it does suggest that there may be real uncertainty about the qualitative differences between the core, edge, and middle environments. The authors do explain that a lack of variation in individual responses to the field experiments would preclude the testing of further hypothesis, but do not mention how a salient lack of variation in novelty/ predictability between the environments could impact their hypotheses.
An assessment/quantification of the rate at which the different populations of grackles encounter novel stimuli would be a cornerstone of the success of this proposed study. Certainly, the authors cannot address this in much more detail during the preprint stage, but they need to consider how to best assess/describe differences before starting the full study. Such an assessment could take the form of either a GIS desktop study (comparing, for example, rates of dam/canal construction in core versus edge sections of the distribution range), or observational/ movement data contrasting how frequently members of core versus edge populations encounter artificial sources of water/food in a given month/year. Considering the long-term nature of the larger project, it is possible that these data are already available, but I am speculating. I would highly recommend that such an assessment be undertaken, beyond the mere mention of expected differences. This would solidify the central idea that there are concrete differences between the environments.
Despite this concern, the authors attended well to the comments and recommendations of the two reviewers – both experts in cognitive ecology. It is a preprint showing clear thinking and a consideration of most of the challenges that may be encountered during the course of the study. My own opinion and the estimations of the two reviewers all underscore the originality and value of this project – this should be a very valuable and potentially novel study. I look forward to seeing the outcomes of the research.

References

[1] McCune, K. B., McElreath, R., and Logan, C. J. (2019). Investigating the use of learning mechanisms in a species that is rapidly expanding its geographic range. In principle recommendation by Peer Community In Ecology. corinalogan.com/Preregistrations/g_sociallearning.html
[2] Benson-Amram, S. and Holekamp, K. E. (2012). Innovative problem solving by wild spotted hyenas. Proceedings of the Royal Society B: Biological Sciences, 279(1744), 4087–4095. doi: 10.1098/rspb.2012.1450
[3] Federspiel, I. G., Boeckle, M., von Bayern, A. M. P. and Emery, N. J. (2019). Exploring individual and social learning in jackdaws (Corvus monedula). Learning & Behavior, 47(3), 258–270. doi: 10.3758/s13420-019-00383-8