Behavioural ecology meets oncology: quantifying the recovery of animal behaviour to a transient exposure to a cancer risk factor

Abstract

Wildlife is increasingly exposed to sublethal transient cancer risk factors, including mutagenic substances, which activates their anti-cancer defences, promotes tumourigenesis, and may negatively impact populations. Little is known about how exposure to cancer risk factors impacts the behaviour of wildlife. Here, we investigated the effects of a sublethal, short-term exposure to a carcinogen at environmentally relevant concentrations on the activity patterns of wild Girardia tigrina planaria during a two-phase experiment, consisting of a 7-day exposure to cadmium period followed by a 7-day recovery period. To comprehensively explore the effects of the exposure on activity patterns, we employed the double hierarchical generalized linear model framework which explicitly models residual intraindividual variability in addition to the mean and variance of the population. We found that exposed planaria were less active compared to unexposed individuals and were able to recover to pre-exposure activity levels albeit with a reduced variance in activity at the start of the recovery phase. Planaria showing high activity levels were less predictable with larger daily activity variations and higher residual variance. Thus, the shift in behavioural variability induced by an exposure to a cancer risk factor can be quantified using advanced tools from the field of behavioural ecology. This is required to understand how tumourous processes affect the ecology of species.

Cancer and One Health: tumor-bearing individuals can act as super spreaders of symbionts in communities

“…Given the diversity of the links between infectious agents and malignant pathologies (Vittecoq et al , 2013;Ewald and Swain Ewald, 2017;Thomas et al , 2017), Dujon et al (M. Dujon et al , 2021) recently advocated for a greater reflection on the integration of cancer into the One Health perspective. For example, it is increasingly accepted that human activities are responsible for an increase in cancers in wildlife (Giraudeau et al , 2018;Sepp et al , 2019;Baines et al , 2021;Klaassen et al , 2024), and this could affect the dynamics of parasite communities, given that cancers often lead to a greater vulnerability to infections through, for instance, immune suppression (Vittecoq et al , 2013;Kareva, 2020;Yürekli, Erbaş1 and 2, 2021). More specifically, Dujon et al (M. Dujon et al , 2021) predicted that cancer pathologies could increase the circulation rate of infectious agents in ecosystems, when hosts harboring tumors become super spreaders which could exacerbate zoonotic risks.…”

The complex effects of modern oncogenic environments on the fitness, evolution and conservation of wildlife species

“…The anti‐cancer defences of an organism encompass multiple layers intended to stop the initiation and progression of malignancies at different stages (Box 2 ). Regardless of the nature of the defences activated, none of them are ultimately without costs; they use energy which cannot be allocated in the other body functions because of trade‐offs (Boutry et al., 2020 ; Jacqueline et al., 2017 ; Klaasen et al., 2024 ). In addition, energy is not the sole cost: apoptosis and/or cellular senescence, which are powerful protective mechanisms against tumorigenesis (DeGregori, 2011 ; Wang et al., 2022 ), are not very costly in terms of energy, but they remove cells that could be involved in normal homeostasis, resulting in indirect costs (Aktipis, 2020 ; Tower, 2015 ).…”

“…To explore this field of research, it could be appropriate to use first models in which we can simulate the appearance of oncogenic mutations (e.g. see for instance Fortunato et al., 2021 ; Klaasen et al., 2024 ) or, even better, cancer, for example by adapting the technologies developed by medical research into anti‐cancer vaccines (Saxena et al., 2021 ; Schumacher & Schreiber, 2015 ) or through activating certain oncogenic pathways using specific mutagens (Dujon, Boutry, Tissot, Meliani, et al., 2022 ). By designing a challenge that exposes animals to proxies of cancer inducers, with the aim of triggering their anti‐cancer defences without inducing malignant tumor growth, we can effectively distinguish the effects of activating anti‐cancer defences from the underlying pathology (see next point).…”