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

Tick-borne pathogens are considered as one of the major threats to public health – Lyme borreliosis being a well-known example of such disease. Global change – from climate change to changes in land use or invasive species – is playing a role in the increased risk associated with these pathogens. An important aspect of our knowledge of ticks and their associated pathogens is seasonality – one component being the phenology of within-year tick occurrences. This is important both in terms of health risk – e.g., when is the risk of encountering ticks high – and ecological understanding, as tick dynamics may depend on the weather as well as different hosts with their own dynamics and habitat use.

Hoch et al. (2023) provide a detailed data set on the phenology of one species of tick, Ixodes ricinus, in 6 different locations of France. Whereas relatively cool sites showed a clear peak in spring-summer, warmer sites showed in addition relatively high occurrences in fall-winter, with a minimum in late summer-early fall. Such results add robust data to the existing evidence of the importance of local climatic patterns for explaining tick phenology.

Recent analyses have shown that the phenology of Lyme borreliosis has been changing in northern Europe in the last 25 years, with seasonal peaks in cases occurring now 6 weeks earlier (Goren et al. 2023). The study by Hoch et al. (2023) is of too short duration to establish temporal changes in phenology (“only” 8 years, 2014-2021, see also Wongnak et al 2021 for some additional analyses; given the high year-to-year variability in weather, establishing phenological changes often require longer time series), and further work is needed to get better estimates of these changes and relate them to climate, land-use, and host density changes. Moreover, the phenology of ticks may also be related to species-specific tick phenology, and different tick species do not respond to current changes in identical ways (see for example differences between the two Ixodes species in Finland; Uusitalo et al. 2022). An efficient surveillance system requires therefore an adaptive monitoring design with regard to the tick species as well as the evolving causes of changes.

References

Goren, A., Viljugrein, H., Rivrud, I. M., Jore, S., Bakka, H., Vindenes, Y., & Mysterud, A. (2023). The emergence and shift in seasonality of Lyme borreliosis in Northern Europe. Proceedings of the Royal Society B: Biological Sciences, 290(1993), 20222420. https://doi.org/10.1098/rspb.2022.2420

Hoch, T., Madouasse, A., Jacquot, M., Wongnak, P., Beugnet, F., Bournez, L., . . . Agoulon, A. (2023). Seasonality of host-seeking Ixodes ricinus nymph abundance in relation to climate. bioRxiv, ver.4 peer-reviewed and recommended by Peer Community In Ecology. https://doi.org/10.1101/2022.07.25.501416

Uusitalo, R., Siljander, M., Lindén, A., Sormunen, J. J., Aalto, J., Hendrickx, G., . . . Vapalahti, O. (2022). Predicting habitat suitability for Ixodes ricinus and Ixodes persulcatus ticks in Finland. Parasites & Vectors, 15(1), 310. https://doi.org/10.1186/s13071-022-05410-8

Wongnak, P., Bord, S., Jacquot, M., Agoulon, A., Beugnet, F., Bournez, L., . . . Chalvet-Monfray, K. (2022). Meteorological and climatic variables predict the phenology of Ixodes ricinus nymph activity in France, accounting for habitat heterogeneity. Scientific Reports, 12(1), 7833. https://doi.org/10.1038/s41598-022-11479-z

What predisposes two individuals to form and maintain a relationship is a fundamental question. Using facial recognition to see whether couples' faces change over time to become more and more similar, psychology researchers have concluded that couples tend to be formed from the start between people whose faces are more similar than average [1]. As the saying goes, birds of a feather flock together.

And what about in nature? Are these rules of assembly valid for communities of different species?

In his seminal contribution, Robert MacArthur (1984) wrote ‘To do science is to search for repeated patterns’ [2]. Identifying the mechanisms that govern the arrangement of life is a hot research topic in the field of ecology for decades, and an absolutely essential prerequisite to answer the outstanding question of what shape ecological patterns in multi-species communities such as species-area relationships, relative species abundances, or spatial and temporal turnover of community composition; amid others [3]. To explain ecological patterns in nature, some rely on the concept that every species - through evolutionary processes and the acquisition of a unique set of traits that allow a species to be adapted to its abiotic and biotic environment - occupies a unique niche: Species coexistence comes as the result of niche differentiation [4,5]. Such a view has been challenged by the recognition of the key role of neutral processes [6], however, in which demographic stochasticity contributes to shape multi-species communities and to explain why congener species coexist much more frequently than expected by chance [7,8]. While the niche-based and neutral theories appear seemingly opposed at first sight [9], the dichotomy may be more philosophical than empirical [4,5]. Many examples have come to support that both concepts are not incompatible as they together influence the structure, diversity and functioning of communities [10], and are simply extreme cases of a continuum [11]. From this perspective, extrinsic factors, i.e., environmental heterogeneity, may influence the location of a given community along the niche-neutrality continuum. 

The walk of species in nature is therefore neither random nor ecologically predestined. In microbial assemblages, the co-existence of these two antagonistic mechanisms has been shown both theoretically and empirically. It has been shown that a combination of stabilising (niche) and equalising (neutral) mechanisms was responsible for the existence of groups of coexistent species (clumps) in a phytoplankton rich community [12]. Analysing interannual changes (2003-2009) in the weekly abundance of diatoms and dinoflagellates located in a temperate coastal ecosystem of the Western English Channel, Mutshinda et al. [13] found a mixture of biomass dynamics consistent with the neutrality-niche continuum hypothesis. While niche processes explained the dynamic of phytoplankton functional groups (i.e., diatoms vs. dinoflagellates) in terms of biomass, neutral processes mainly dominated - 50 to 75% of the time - the dynamics at the species level within functional groups [13]. From one endpoint to another, defining the location of a community along the continuum is all matter of scale [4,11].

In their study, testing predictions made by an emergent neutrality model, Graco-Roza et al. [14] provide empirical evidence that neutral and niche processes joined together to shape and drive planktonic communities in a riverine ecosystem. Body size - the 'master trait' - is used here as a discriminant ecological dimension along the niche axis. From their analysis, they not only show that the specific abundance is organised in clumps and gaps along the niche axis, but also reveal that different clumps exist along the river course. They identify two main clumps in body size - with species belonging to three different morphologically-based functional groups - and characterise that among-species differences in biovolume are driven by functional redundancy at the clump level; species functional distinctiveness being related to the relative biovolume of species. By grouping their variables according to seasons (cold-dry vs. warm-wet) or river elevation profile (upper, medium and lower course), they hereby highlight how environmental heterogeneity contributes to shape species assemblages and their dynamics and conclude that emergent neutrality models are a powerful approach to explain species coexistence; and therefore ecological patterns.

References

[1] Tea-makorn PP, Kosinski M (2020) Spouses’ faces are similar but do not become more similar with time. Scientific Reports, 10, 17001. https://doi.org/10.1038/s41598-020-73971-8.

[2] MacArthur RH (1984) Geographical Ecology: Patterns in the Distribution of Species. Princeton University Press.

[3] Vellend M (2020) The Theory of Ecological Communities (MPB-57). Princeton University Press.

[4] Wennekes PL, Rosindell J, Etienne RS (2012) The Neutral—Niche Debate: A Philosophical Perspective. Acta Biotheoretica, 60, 257–271. https://doi.org/10.1007/s10441-012-9144-6.

[5] Gravel D, Guichard F, Hochberg ME (2011) Species coexistence in a variable world. Ecology Letters, 14, 828–839. https://doi.org/10.1111/j.1461-0248.2011.01643.x.

[6] Hubbell SP (2001) The Unified Neutral Theory of Biodiversity and Biogeography (MPB-32). Princeton University Press.

[7] Leibold MA, McPeek MA (2006) Coexistence of the Niche and Neutral Perspectives in Community Ecology. Ecology, 87, 1399–1410. https://doi.org/10.1890/0012-9658(2006)87[1399:COTNAN]2.0.CO;2.

[8] Pielou EC (1977) The Latitudinal Spans of Seaweed Species and Their Patterns of Overlap. Journal of Biogeography, 4, 299–311. https://doi.org/10.2307/3038189.

[9] Holt RD (2006) Emergent neutrality. Trends in Ecology & Evolution, 21, 531–533. https://doi.org/10.1016/j.tree.2006.08.003. 

[10] Scheffer M, Nes EH van (2006) Self-organized similarity, the evolutionary emergence of groups of similar species. Proceedings of the National Academy of Sciences, 103, 6230–6235. https://doi.org/10.1073/pnas.0508024103.

[11] Gravel D, Canham CD, Beaudet M, Messier C (2006) Reconciling niche and neutrality: the continuum hypothesis. Ecology Letters, 9, 399–409. https://doi.org/10.1111/j.1461-0248.2006.00884.x.

[12] Vergnon R, Dulvy NK, Freckleton RP (2009) Niches versus neutrality: uncovering the drivers of diversity in a species-rich community. Ecology Letters, 12, 1079–1090. https://doi.org/10.1111/j.1461-0248.2009.01364.x.

[13] Mutshinda CM, Finkel ZV, Widdicombe CE, Irwin AJ (2016) Ecological equivalence of species within phytoplankton functional groups. Functional Ecology, 30, 1714–1722. https://doi.org/10.1111/1365-2435.12641.

[14] Graco-Roza C, Segura AM, Kruk C, Domingos P, Soininen J, Marinho MM (2021) Clumpy coexistence in phytoplankton: The role of functional similarity in community assembly. bioRxiv, 869966, ver. 6 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/869966

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

Most, if not all, predators consume carrion in some circumstances (Sebastián-Gonzalez et al. 2023). Consequently, significant fluctuations in carrion availability can impact predator-prey dynamics by altering the ratio of carrion to live prey in the predators' diet (Roth 2003). Changes in carrion availability may lead to reduced predation when carrion is more abundant (hypo-predation) and intensified predation if predator populations surge in response to carrion influxes but subsequently face scarcity (hyper-predation), (Moleón et al. 2014, Mellard et al. 2021). However, this relationship between predation and scavenging is often challenging because of the lack of empirical data.
 
In the study conducted by Sidous et al. (2024), they used a large database on the abundance of spotted hyenas and their prey in Zimbabwe and Multivariate Autoregressive State-Space Models to calculate hyena and prey population densities and trends over a 60-year span. The researchers took advantage of abrupt fluctuations in elephant carcass availability that produced alternating periods of high and low carrion availability related to changing management strategies (i.e., elephant culling and water supply).
 
Interestingly, their analyses reveal a coupling of predator and prey densities over time, but they do not detect an effect of carcass availability on predator and prey dynamics. However, the density of prey and hyena was partially driven by the different temporal periods, suggesting some subtle effects of carrion availability on population trends. While it is acknowledged that other variables likely impact the population dynamics of hyenas and their prey, this is the first attempt to understand the influence of carrion pulses on predator-prey interactions across an extensive temporal scale. I hope this helps to establish a new research line on the effect of large carrion pulses, as this is currently largely understudied, even though the occurrence of carrion pulses, such as mass mortality events, is expected to increase over time (Fey et al. 2015).
 
References
 
Courchamp, F. et al. 2000. Rabbits killing birds: modelling the hyperpredation process. J. Anim. Ecol. 69: 154-164.
https://doi.org/10.1046/j.1365-2656.2000.00383.x

Fey, S. B. et al. 2015. Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events. PNAS 112: 1083-1088.
https://doi.org/10.1073/pnas.1414894112
 
Mellard, J. P. et al. 2021. Effect of scavenging on predation in a food web. Ecol. Evol. 11: 6742- 6765.
https://doi.org/10.1002/ece3.7525

Moleón, M. et al. 2014. Inter-specific interactions linking predation and scavenging in terrestrial vertebrate assemblages. Biol. Rev. Camb. Philos. Soc. 89: 1042-1054.
https://doi.org/10.1111/brv.12097
 
Roth, J. 2003. Variability in marine resources affects arctic fox population dynamics. J. Anim. Ecol. 72: 668-676.
https://doi.org/10.1046/j.1365-2656.2003.00739.x
 
Sebastián-González, E. et al. 2023. The underestimated role of carrion in diet studies. Global Ecol. Biogeogr. 32: 1302-1310.
https://doi.org/10.1111/geb.13707
 
Sidous, M. et al. 2024. Insights on the effect of mega-carcass abundance on 1 the population dynamics of a facultative scavenger predator and its prey. bioRxiv, ver. 2 peer-reviewed and recommended by PCI Ecology.
https://doi.org/10.1101/2023.11.08.566247