Transgenerational exposure to deoxygenation and warming disrupts mate detection in Gammarus locusta
Creators: name: Pereira, Beatriz
name: Neff, Simon
name: Borges, Francisco
name: Otjacques, Eve
name: Barreto, Guilherme
name: Ranucci, Maddalena
name: Court, Melanie
name: Rosa, Rui
name: Repolho, Tiago
name: Paula, José Ricardo
Publisher: name: Zenodo
Year: 2023
Subjects: subject: Ecology
subject: FOS: Biological sciences
subject: Climate change
subject: reproductive behavior
subject: amphipod
subject: gammarid
subject: carry-over effects

description: Ocean deoxygenation and warming have been shown to pose a growing threat to the health of marine organisms and ecosystems. Yet, the potential for acclimation and adaptation remains poorly understood. The aim of this study was to evaluate the effects of transgenerational exposure to reduced oxygen availability and elevated seawater temperature on the chemosensory-dependent mating mechanisms of male amphipods Gammarus locusta. Three subsequent generations were exposed to four experimental treatments for 30 days: i) present-day scenario, ii) warming; iii) deoxygenation; and iv) warming+deoxygenation. After exposure, the number of individuals that reached adulthood was gauged, and adult males from F0 and F1 were subjected to behavioral trials to assess their capacity of long-distance female cue detection through quantification of response time, first direction of movement, activity rate, and proportion of time spent in female scent cues. Ocean-warming-induced mortality and reduced oxygen availability had adverse effects on each of the investigated behavioral traits, which were amplified when combined with elevated temperature. Still, when compared to F0, the F1 generation demonstrated more adaptability (i.e., higher activity rate and preference for female odors) to the combination of the two stressors, suggesting positive carry-over effects. Nevertheless, full recovery to control levels was not observed. Altogether, this study indicates that future scenarios of ocean deoxygenation and warming have the potential to disrupt chemosensory-dependent mate detection in amphipods, but also suggests possible behavioral adaptations. We call for greater research efforts on long-term impacts of ocean change on the behavioral and physiological processes of benthic coastal communities.
description: Funding provided by: Programa Operacional Regional de Lisboa, Portugal 2020*Crossref Funder Registry ID: Award Number: LISBOA- 01-0145-FEDER-028609
Funding provided by: Fundação para a Ciência e TecnologiaCrossref Funder Registry ID: https://ror.org/00snfqn58Award Number: UIDB/04292/2020
Funding provided by: Fundação para a Ciência e TecnologiaCrossref Funder Registry ID: https://ror.org/00snfqn58Award Number: LA/P/0069/2020
Funding provided by: Fundação para a Ciência e TecnologiaCrossref Funder Registry ID: https://ror.org/00snfqn58Award Number: DL57/2016/CP1479/CT0023
Funding provided by: Fundação para a Ciência e TecnologiaCrossref Funder Registry ID: https://ror.org/00snfqn58Award Number: SFRH/BD/147294/2019
Funding provided by: Fundação para a Ciência e TecnologiaCrossref Funder Registry ID: https://ror.org/00snfqn58Award Number: UI/BD/151019/2021
Funding provided by: Fundação para a Ciência e TecnologiaCrossref Funder Registry ID: https://ror.org/00snfqn58Award Number: PTDC/BIA-BMA/28609/2017
Funding provided by: Fundação para a Ciência e TecnologiaCrossref Funder Registry ID: https://ror.org/00snfqn58Award Number: 2021.01030.CEECIND
Funding provided by: European UnionCrossref Funder Registry ID: https://ror.org/019w4f821Award Number: LISBOA- 01-0145-FEDER-028609
Funding provided by: Fundação para a Ciência e TecnologiaCrossref Funder Registry ID: https://ror.org/00snfqn58Award Number: 2021.06590.BD
description: Our study aimed to investigate the transgenerational effects of increased temperature and lower oxygen levels on male gammarids' response to female scent signals. For this purpose, we conducted a binary-choice experiment using a total of 30 males from the F0 generation and 26 males from the F1 generation. These trials involved direct observations, during which we recorded four key traits of male individuals: response time (time to initiate movement towards an association zone), proportion of first choice (initial movement towards the female-scented association zone), cumulative time spent in each association zone, and activity rate (proportion of time spent actively moving). 

Data analysis of behavioral outputs was performed through generalized linear mixed models (GLMM) using the negative binomial (number of individuals, response time), binomial (first choice), and Gaussian (cumulative time & activity rate) residual distributions. All models used temperature, oxygen, and generation as categorical fixed factors, and replicate ID as random factors. Transgenerational effects of the treatments on these variables were considered whenever an interacting effect was observed between Generation and Treatment. Full models, with all possible interactions, were tested using the function 'glmmTMB' from the package 'glmmTMB' and the function 'Anova' from the package 'car' in R, version 3.4.3. Post-hoc multiple comparisons were performed using the package 'emmeans' and applying Tukey corrections. Model assumptions and performance were validated using the package "performance". Data exploration was conducted using the HighstatLibV10 R library from Highland Statistics.