"The noble false widow spider Steatoda nobilis is an emerging public health and ecological threat" by Clive Hambler (2020) is an appealing article discussing important aspects of the ecology and distribution of a medically significant spider, and the health concerns it raises.
By contrast to previous studies (Dunbar et al., 2018; Warell et al., 1991; Bauer et al., 2019; BBC 2013, 2018), this article, with its extensive media and scientific literature review, shows that S. nobilis (Thorell, 1875) is now an important health concern in Britain. Indeed, the author shows that the population of this spider has significantly increased, at least since 1990, in both southern Britain and Ireland where it has remained greatly under-recorded. In these areas, S. nobilis is now often the dominant spider on and in buildings, in places in which there is a high a risk of bites, some of which are likely to be severe, in humans, with these bites largely under-recorded. According to Clive Hambler "There is thus a possibility of bites being left without adequate rapid treatment and monitoring - with a low but non-trivial risk of necrosis or sepsis".
The author points that one of the reasons for the lack of awareness of the risk is that arachnologists typically have a conflict of interest between the conservation of the species they study and raising concerns about spiders. This may lead them to understate the risk. Clive Hambler therefore calls for a closer, appropriately weighted attention to the frequency and risk of bites, based on all the information available, rather than being "dismissive of the possibilities of bites and impacts simply because many media reports contain major errors or alarmism". He also argues that the British Arachnological Society’s guidance on "false widow spiders" "needs substantive revision, both in terms of the likelihood of bites and the severity of effects."
Indeed, the author demonstrates that many inaccuracies have been published (see Table 3 of his manuscript) and, for each, he provides a correction and/or an alternative opinion. At the end of this MS (see Table 4), he provides testable speculations and hypotheses. As he rightly points out, testing is very important to fuel the debate, because "It will be very difficult to get a balanced and proportionate debate and response for such a confused and emotive issue, especially with the many misleading popular reports." He also suggests that research will require interdisciplinary collaboration between experts in many domains, including pathologists, immunologists, clinicians, ecologists, arachnologists, psychologists, physiologists, climatologists and epidemiologists.
This preprint is clearly descriptive and speculative, but well-written, interesting and certainly useful in terms of a review of the biology, ecology, potential dangerousness and distribution of S. nobilis, particularly for future studies. There is no doubt that arachnologists, the medical community and the media will be interested in this article, which is intended to sound the alarm. Naturalists in general will also be interested in this manuscript because it is an original and successful attempt to increase knowledge about a particular taxon based on diverse information sources.
The structure of the MS is a bit odd, with a certain toing-and-froing between the ecology/biology/distribution of the spider and the risks, dangerousness and venom of bites, but this is not problematic, as shown by the reviews of the manuscript - three reviews (available below) were written, two by specialists in this noble false widow (Michel Dugon and another researcher who wished to remain anonymous).
Despite the controversy surrounding certain of the statements made in this article, I therefore strongly recommend it and look forward to seeing the identified research priorities addressed.

References

[1] Hambler, C. (2020). The “Noble false widow” spider Steatoda nobilis is an emerging public health and ecological threat. OSF Preprints, axbd4, ver. 4 peer-reviewed and recommended by PCI Zoology. doi: 10.31219/osf.io/axbd4
[2] Dunbar J.P., Afoullouss S., Sulpice R., Dugon M.M. (2018) Envenomation by the noble false widow spider Steatoda nobilis (Thorell, 1875) - five new cases of steatodism from Ireland and Great Britain. Clin Toxicol (Phila). 56(6):433-435. doi: 10.1080/15563650.2017.1393084
[3] Warrell D.A., Shaheen J., Hillyard P.D., Jones D. (1991) Neurotoxic envenoming by an immigrant spider (Steatoda nobilis) in southern England. Toxicon. 29(10):1263-5. doi: 10.1016/0041-0101(91)90198-Z
[4] Bauer, T., Feldmeier, S., Krehenwinkel, H., Wieczorrek, C., Reiser, N. and Dreitling, R. (2019) Steatoda nobilis, a false widow on the rise: a synthesis of past and current distribution trends. NeoBiota 42: 19–43. doi: 10.3897/neobiota.42.31582
[5] BBC (2013). False widow spider bites footballer Steve Harris. http://www.bbc.co.uk/news/uk-england-devon-24470023 Accessed 1 November 2018.
[6] BBC (2018). False widow spider infestation schools to remain shut. https://www.bbc.co.uk/news/uk-england-london-45761046 Accessed 19 December 2018.

The popularity of iNaturalist and other online biodiversity databases to which the general public and specialists alike contribute observations has skyrocketed in recent years (Dance 2022). The AI-based algorithms (computer vision) which provide the first identification of a given organism on an uploaded photograph have become very sophisticated, suggesting initial identifications often down to species level with a surprisingly high degree of accuracy. The initial identifications are then confirmed or improved by feedback from the community, which works particularly well for organismal groups to which many active community members contribute, such as the birds. Hence, providing initial observations and identifying observations of others, as well as browsing the recorded biodiversity for given locales or the range of occurrences of individual taxa has become a meaningful and satisfying experience for the interested naturalist. Furthermore, several research studies have now been published relying on observations uploaded to iNaturalist (Szentivanyi and Vincze 2022). However, using the enormous amount of natural history data available on iNaturalist in a systematic way has remained challenging, since this requires not only retrieving numerous observations from the database (in the hundreds or even thousands), but also some level of transparent quality control.

Billotte (2022) provides a protocol and R scripts for the quality assessment of downloaded observations from iNaturalist, allowing an efficient and reproducible stepwise approach to prepare a high-quality data set for further analysis. First, observations with their associated metadata are downloaded from iNaturalist, along with the corresponding entries from the Global Biodiversity Information Facility (GBIF). In addition, a taxonomic reference list is obtained (these are available online for many taxa), which is used to assess the taxonomic consistency in the dataset. Second, the geo-tagging is assessed by comparing the iNaturalist and GBIF metadata. Lastly, the image quality is assessed using pyBRISQUE. The approach is illustrated using spiders (Araneae) as an example. Spiders are a very diverse taxon and an excellent taxonomic reference list is available (World Spider Catalogue 2022). However, spiders are not well known to most non-specialists, and it is not easy to take good pictures of spiders without using professional equipment. Therefore, the ability of iNaturalist’s computer vision to provide identifications is limited to this date and the community of specialists active on iNaturalist is comparatively small. Hence, spiders are a good taxon to demonstrate how the pipeline results in a quality-controlled dataset based on crowed-sourced data. Importantly, the software employed is free to use, although inevitably, the initial learning curve to use R scripts can be steep, depending on prior expertise with R/RStudio. Furthermore, the approach is employable with databases other than iNaturalist.

In summary, Billotte's (2022) pipeline allows researchers to use the wealth of observations on iNaturalist and other databases to produce large metadata and image datasets of high-quality in a reproducible way. This should pave the way for more studies, which could include, for example, the assessment of range expansions of invasive species or the evaluation of the presence of endangered species, potentially supporting conservation efforts.

References

Billotte J (2022) A pipeline for assessing the quality of images and metadata from crowd-sourced databases. BiorXiv, 2022.04.29.490112, ver 5 peer reviewed and recommended by Peer Community In Zoology. https://doi.org/10.1101/2022.04.29.490112

Dance A (2022) Community science draws on the power of the crowd. Nature, 609, 641–643. https://doi.org/10.1038/d41586-022-02921-3

Szentivanyi T, Vincze O (2022) Tracking wildlife diseases using community science: an example through toad myiasis. European Journal of Wildlife Research, 68, 74. https://doi.org/10.1007/s10344-022-01623-5

World Spider Catalog (2022). World Spider Catalog. Version 23.5. Natural History Museum Bern, online at http://wsc.nmbe.ch. https://doi.org/10.24436/2

Biotic interactions are often shaped by abiotic factors (Liu and Gaines 2022). Although this notion is not new in ecology and evolutionary biology, we are still far from a thorough understanding of how biotic interactions change along abiotic gradients in space and time. This is particularly challenging because abiotic factors can affect organisms and their interactions in multiple – direct or indirect – ways. For example, because abiotic conditions strongly determine how energy enters biological systems via producers, their effects can propagate through entire food webs, from the bottom to the top (O’Connor 2009, Gilbert et al 2019). Understanding how biological diversity - both within and across species - is shaped by the indirect effects of environmental conditions is a timely question as climate change and anthropogenic activities have been altering temperature and water availability across different ecosystems.

Motivated by the current water crisis and severe droughts predicted for the near future worldwide (du Plessis 2019), Migeon et al. (2023) investigated how water limitation on producers scales up to affect life-history patterns of a widespread crop pest, the spider mite Tetranychus urticae. The authors sampled spider mite populations (n = 12) along a striking gradient of climatic conditions (>16 degrees of latitude) in Europe. After letting mites acclimate to lab conditions for several generations, the authors performed a common garden experiment to quantify how the life-history traits of mite populations from different locations respond to drought stress in their host plants.

Curiously, the authors found that, when reared on drought-stressed plants, mites tended to develop faster, had higher fecundity and lower dispersion rates. This response was in line with some results obtained previously with Tetranychus species (e.g. Ximénez-Embun et al 2016). Importantly, despite some experimental caveats in the experimental design, which makes it difficult to completely disentangle the specific effects of location vs. environmental noise, results suggest the climate that populations originally experienced was also an important determinant of the plastic response in these herbivores. In fact, populations from wetter and colder regions showed a steeper change in drought response, while populations from arid climates showed a shallower response. This interesting result suggests the importance of intraspecific (between-populations) variation in the response to drought, which might be explained by the climatic heterogeneity in space throughout the evolutionary history of different populations. These results become even more important in our rapidly changing world, highlighting the importance of considering genetic variation (and conditions that generate it) when predicting plastic and evolutionary responses to stressful conditions.
 
REFERENCES

du Plessis, A. (2019). Current and Future Water Scarcity and Stress. In: Water as an Inescapable Risk. Springer Water. Springer, Cham. https://doi.org/10.1007/978-3-030-03186-2
 
Gibert, J.P. Temperature directly and indirectly influences food web structure. Sci Rep 9, 5312 (2019). https://doi.org/10.1038/s41598-019-41783-0
 
Liu, O. R., & Gaines, S. D. (2022). Environmental context dependency in species interactions. Proceedings of the National Academy of Sciences, 119(36), e2118539119. https://doi.org/10.1073/pnas.2118539119
 
Migeon A., Auger P., Fossati-Gaschignard O., Hufbauer R.A, Miranda M., Zriki G., Navajas M. (2023) The response to drought-stressed host plants varies among herbivorous mite populations from a climate gradient. bioRxiv, 2021.10.21.465244, ver. 4 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2021.10.21.465244
 
O'Connor, M.I. (2009), Warming strengthens an herbivore-plant interaction. Ecology, 90: 388-398. https://doi.org/10.1890/08-0034.1
 
Ximénez-Embún, M. G., Ortego, F., & Castañera, P. (2016). Drought-stressed tomato plants trigger bottom-up effects on the invasive Tetranychus evansi. PloS one, 11(1), e0145275. https://doi.org/10.1371/journal.pone.0145275

The intricate relationships between parasites and their hosts often involve a choreography of behavioral changes, with parasites manipulating their hosts in a way that enhances - or seemingly enhances – their transmission (Hughes et al., 2012; Moore, 2002; Poulin, 2010). Host manipulation is increasingly acknowledged as a pervasive adaptive transmission strategy employed by parasites, and as such is one of the most remarkable manifestations of the extended phenotype (Dawkins, 1982).

In this laboratory study, Rigaud et al. (2023) delved into the time course of antipredator behavioral modifications induced by the acanthocephalan Pomphorhynchus laevis in its amphipod intermediate host Gammarus pulex. This system has a good foundation of prior knowledge (Bakker et al., 2017; Fayard et al., 2020; Perrot-Minnot et al., 2023), nicely drawn upon for the present work. This parasite orchestrates a switch from predation suppression, during the noninfective phase, to predation enhancement upon maturation. Specifically, G. pulex infected with the non-infective acanthella stage of the parasite can exhibit increased refuge use and reduced activity compared to uninfected individuals (Dianne et al., 2011, 2014), leading to decreased predation by trout (Dianne et al., 2011). In contrast, upon reaching the infective cystacanth stage, the parasite can enhance the susceptibility of its host to trout predation (Dianne et al., 2011).

The present work aimed to understand the temporal sequence of these behavioral changes across the entire ontogeny of the parasite. The results confirmed the protective role of P. laevis during the acanthella stage, wherein infected amphipods exhibited heightened refuge use. This protective manipulation, however, became significant only later in the parasite's ontogeny, suggesting a delayed investment strategy, possibly influenced by the extended developmental time of P. laevis. The protective component wanes upon reaching the cystacanth stage, transitioning into an exposure strategy, aligning with theoretical predictions and previous empirical work (Dianne et al., 2011; Parker et al., 2009). The switch was behavior-specific. Unlike the protective behavior, a decline in the amphipod activity rate manifested early in the acanthella stage and persisted throughout development, suggesting potential benefits of reduced activity for the parasite across multiple stages. Furthermore, the findings challenge previous assumptions regarding the condition-dependency of manipulation, revealing that the parasite-induced behavioral changes predominantly occurred in the presence of cues signaling potential predators. Finally, while amphipods infected with acanthella stages displayed survival rates comparable to their uninfected counterparts, increased mortality was observed in those infected with cystacanth stages.

Understanding the temporal sequence of host behavioral changes is crucial for deciphering whether it is adaptive to the parasite or not. This study stands out for its meticulous examination of multiple behaviors over the entire ontogeny of the parasite highlighting the complexity and condition-dependent nature of manipulation. The protective-then-expose strategy emerges as a dynamic process, finely tuned to the developmental stages of the parasite and the ecological challenges faced by the host. The delayed emergence of protective behaviors suggests a strategic investment by the parasite, with implications for the host's survival and the parasite's transmission success. The differential impact of infection on refuge use and activity rate further emphasizes the need for a multidimensional approach in studying parasitic manipulation (Fayard et al., 2020). This complexity demands further exploration, particularly in deciphering how trophically-transmitted parasites shape the behavioral landscape of their intermediate hosts and its temporal dynamic (Herbison, 2017; Perrot-Minnot & Cézilly, 2013).  As we discover the many subtleties of these parasitic manipulations, new avenues of research are unfolding, promising a deeper understanding of the ecology and evolution of host-parasite interactions.

References

Bakker, T. C. M., Frommen, J. G., & Thünken, T. (2017). Adaptive parasitic manipulation as exemplified by acanthocephalans. Ethology, 123(11), 779–784. https://doi.org/10.1111/eth.12660

Dawkins, R. (1982). The extended phenotype: The long reach of the gene (Reprinted). Oxford University Press.

Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Gaillard, M., Léger, E., & Rigaud, T. (2011). Protection first then facilitation: A manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution, 65(9), 2692–2698. https://doi.org/10.1111/j.1558-5646.2011.01330.x

Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Guvenatam, A., & Rigaud, T. (2014). Parasite-induced alteration of plastic response to predation threat: Increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis. International Journal for Parasitology, 44(3–4), 211–216. https://doi.org/10.1016/j.ijpara.2013.11.001

Fayard, M., Dechaume‐Moncharmont, F., Wattier, R., & Perrot‐Minnot, M. (2020). Magnitude and direction of parasite‐induced phenotypic alterations: A meta‐analysis in acanthocephalans. Biological Reviews, 95(5), 1233–1251. https://doi.org/10.1111/brv.12606

Herbison, R. E. H. (2017). Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation. Frontiers in Ecology and Evolution, 5, 102. https://doi.org/10.3389/fevo.2017.00102

Hughes, D. P., Brodeur, J., & Thomas, F. (2012). Host manipulation by parasites. Oxford university press.

Moore, J. (2002). Parasites and the behavior of animals. Oxford University Press.

Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K., & Milinski, M. (2009). When should a trophically transmitted parasite manipulate its host? Evolution, 63(2), 448–458. https://doi.org/10.1111/j.1558-5646.2008.00565.x

Perrot-Minnot, M.-J., & Cézilly, F. (2013). Investigating candidate neuromodulatory systems underlying parasitic manipulation: Concepts, limitations and prospects. Journal of Experimental Biology, 216(1), 134–141. https://doi.org/10.1242/jeb.074146

Perrot-Minnot, M.-J., Cozzarolo, C.-S., Amin, O., Barčák, D., Bauer, A., Filipović Marijić, V., García-Varela, M., Servando Hernández-Orts, J., Yen Le, T. T., Nachev, M., Orosová, M., Rigaud, T., Šariri, S., Wattier, R., Reyda, F., & Sures, B. (2023). Hooking the scientific community on thorny-headed worms: Interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala. Parasite, 30, 23. https://doi.org/10.1051/parasite/2023026

Poulin, R. (2010). Parasite Manipulation of Host Behavior. In Advances in the Study of Behavior (Vol. 41, pp. 151–186). Elsevier. https://doi.org/10.1016/S0065-3454(10)41005-0

Rigaud, T., Balourdet, A., & Bauer, A. (2023). Time-course of antipredator behavioral changes induced by the helminth Pomphorhynchus laevis in its intermediate host Gammarus pulex: The switch in manipulation according to parasite developmental stage differs between behaviors. bioRxiv, ver. 6 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2023.04.25.538244

The critical role that gut microbiota play in many aspects of an animal’s life, including pathogen resistance, detoxification, digestion, and nutritional physiology, is becoming more and more apparent (Engel and Moran 2013; Lindsay et al., 2020). Gut microbiota recruitment and maintenance can be largely affected by the surrounding environment (Chandler et al., 2011; Callens et al., 2020). The environment may thus dictate gut microbiota composition and diversity, which in turn can affect organismal responses to stress. Only few studies have, however, taken the gut microbiota into account to estimate life histories in response to multiple stressors in aquatic systems (Macke et al., 2016). 

Houwenhuyse et al., investigate how the microbiome affects life histories in response to ecologically relevant single and multiple biotic stressors (an oomycete-like parasite, and a toxic cyanobacterium) in Daphnia magna (Houwenhuyse et al., 2023). Daphnia is an excellent model, because this aquatic system lends itself extremely well for gut microbiota transplantation and manipulation. This is due to the possibility to sterilize eggs (making them free of bacteria), horizontal transmission of bacteria from the environment, and the relative ease of culturing genetically similar Daphnia clones in large numbers. 

The authors use an elegant experimental design to show that the Daphnia gut microbial community differs when derived from a laboratory versus natural inoculum, the latter being more diverse. The authors subsequently show that key life history traits (survival, fecundity, and body size) depend on the stressors (and combination thereof), the microbiota (structure and diversity), and Daphnia genotype. A key finding is that Daphnia exposed to both biotic stressors show an antagonistic interaction effect on survival (being higher), but only in individuals containing laboratory gut microbiota. The exact mechanism remains to be determined, but the authors propose several interesting hypotheses as to why Daphnia with more diverse gut microbiota do less well. This could be due, for example, to increased inter-microbe competition or an increased chance of contracting opportunistic, parasitic bacteria. For Daphnia with less diverse laboratory gut microbiota, a monopolizing species may be particularly beneficial for stress tolerance. Alongside these interesting findings, the paper also provides extensive information about the gut microbiota composition (available in the supplementary files), which is a very useful resource for other researchers. 

Overall, this study reveals that multiple, interacting factors affect the performance of Daphnia under stressful conditions. Of importance is that laboratory studies may be based on simpler microbiota systems, meaning that stress responses measured in the laboratory may not accurately reflect what is happening in nature. 

REFERENCES

Callens M, De Meester L, Muylaert K, Mukherjee S, Decaestecker E. The bacterioplankton community composition and a host genotype dependent occurrence of taxa shape the Daphnia magna gut bacterial community. FEMS Microbiology Ecology. 2020;96(8):fiaa128. https://doi.org/10.1093/femsec/fiaa128

Chandler JA, Lang JM, Bhatnagar S, Eisen JA, Kopp A. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLOS Genetics. 2011;7(9):e1002272. https://doi.org/10.1371/journal.pgen.1002272

Engel P, Moran NA. The gut microbiota of insects - diversity in structure and function. FEMS Microbiology Reviews. 2013;37(5):699-735. https://doi.org/10.1111/1574-6976.12025

Houwenhuyse S, Bulteel L, Vanoverberghe I, Krzynowek A, Goel N et al. Microbiome mediated tolerance to biotic stressors: a case study of the interaction between a toxic cyanobacterium and an oomycete-like infection in Daphnia magna. 2023. OSF, ver. 2 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.31219/osf.io/9n4mg

Lindsay EC, Metcalfe NB, Llewellyn MS. The potential role of the gut microbiota in shaping host energetics and metabolic rate. Journal of Animal Ecology. 2020;89(11):2415-2426. https://doi.org/10.1111/1365-2656.13327

Macke E, Tasiemski A, Massol F, Callens M, Decaestecker E. Life history and eco-evolutionary dynamics in light of the gut microbiota. Oikos. 2017;126(4):508-531. https://doi.org/10.1111/oik.03900