Francisco de Oliveira Martins da Camara Borges
@aimmportugal.org
Senior Researcher
AIMM - Marine and Environnment Research Association
I am a Marine Ecologist/Biologist with vast experience in both experimental biology and ecological modelling, primarily in the field of marine climate change and its effects and impacts across marine taxa (e.g., including invertebrates such as cephalopods and ascidians, fish and dolphins, microalgae, and intertidal saltmarsh species). Most of my scientific background (2016-2023) has been developed at the Laboratório Marítimo da Guia, which belongs to the Marine and Environmental Sciences Centre of the Faculty of Sciences of the University of Lisbon (MARE-FCUL). I am currently a Senior Researcher at AIMM - Marine and Environment Research Association, mainly responsible with data analysis and ecological modelling focused on cetacean species.
My PhD (submitted in October 2023 and defended in May 2024), focused on the impacts of marine climate change on Cephalopod species.
I have vast experience in data analysis and statistics, mainly using R studio.
EDUCATION
2024 - PhD in Biology, Marine Biology and Aquaculture, by the Faculty of Sciences of the University of Lisbon
2017 - MSc in Marine Ecology by the Faculty of Sciences of the University of Lisbon
2015 - BSc in Biology - specialization in Environmental (marine) biology, by the Faculty of Sciences of the University of Lisbon
RESEARCH, TEACHING, or OTHER INTERESTS
Aquatic Science, Ecology, Evolution, Behavior and Systematics, Ecology, Ecological Modeling
Scopus Publications
Scholar Citations
Scholar h-index
Scholar i10-index
Scopus Publications
Rui Rosa, Michael Amor, Francisco Borges, Ian G. Gleadall, Vasco Pissarra, Roger Villanueva, Janet R. Voight, and Christian M. Ibáñez
Elsevier
Rui Rosa, Catarina P. Santos, Francisco Borges, Piero Amodio, Michael Amor, John R. Bower, Roy L. Caldwell, Anna Di Cosmo, Melanie Court, Graziano Fiorito,et al.
Beatriz P Pereira, Simon Neff, Francisco O Borges, Eve Otjacques, Guilherme Barreto, Maddalena Ranucci, Mélanie Court, Rui Rosa, Tiago Repolho, and José Ricardo Paula
Oxford University Press (OUP)
Abstract 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: 1) present-day scenario, 2) warming; 3) deoxygenation; and 4) 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, the 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 with 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.
Francisco O Borges, Eduardo Sampaio, Catarina P Santos, and Rui Rosa
Oxford University Press (OUP)
Synopsis Aside from being one of the most fascinating groups of marine organisms, cephalopods play a major role in marine food webs, both as predators and as prey, while representing key living economic assets, namely for artisanal and subsistence fisheries worldwide. Recent research suggests that cephalopods are benefitting from ongoing environmental changes and the overfishing of certain fish stocks (i.e., of their predators and/or competitors), putting forward the hypothesis that this group may be one of the few “winners” of climate change. While many meta-analyses have demonstrated negative and overwhelming consequences of ocean warming (OW), acidification (OA), and their combination for a variety of marine taxa, such a comprehensive analysis is lacking for cephalopod molluscs. In this context, the existing literature was surveyed for peer-reviewed articles featuring the sustained (≥24 h) and controlled exposure of cephalopod species (Cephalopoda class) to these factors, applying a comparative framework of mixed-model meta-analyses (784 control-treatment comparisons, from 47 suitable articles). Impacts on a wide set of biological categories at the individual level (e.g., survival, metabolism, behavior, cell stress, growth) were evaluated and contrasted across different ecological attributes (i.e., taxonomic lineages, climates, and ontogenetic stages). Contrary to what is commonly assumed, OW arises as a clear threat to cephalopods, while OA exhibited more restricted impacts. In fact, OW impacts were ubiquitous across different stages of ontogeny, taxonomical lineages (i.e., octopuses, squids, and cuttlefish). These results challenge the assumption that cephalopods benefit from novel ocean conditions, revealing an overarching negative impact of OW in this group. Importantly, we also identify lingering literature gaps, showing that most studies to date focus on OW and early life stages of mainly temperate species. Our results raise the need to consolidate experimental efforts in a wider variety of taxa, climate regions, life stages, and other key environmental stressors, such as deoxygenation and hypoxia, to better understand how cephalopods will cope with future climate change.
Miguel Fernandes Guerreiro, Francisco Oliveira Borges, Catarina Pereira Santos, José Carlos Xavier, Henk-Jan Hoving, and Rui Rosa
Springer Science and Business Media LLC
AbstractClimate change is expected to have major negative effects on marine life across phylogenetic groups. Cephalopods, however, have life history characteristics that suggest they may benefit from certain climate change scenarios. Of all cephalopods, squids reach the greatest biomasses; as a result, they are of substantial importance for human and predator consumption. To test the hypothesis that the effects of climate change are beneficial for commercial squid, we used species distribution models on climate scenarios for the period between 2000 and 2014, as well as the years 2050 and 2100 (RCP [representative concentration pathway] 2.6, 4.5, 6.0, and 8.5; CMIP5). Our results suggest that consequences of climate change scenarios are species specific. In the North Pacific and Northwest Atlantic, squid’s habitat suitability may increase (from + 0.83% [Doryteuthis pealeii] to + 8.77% increase [Illex illecebrosus]), while it is predicted to decrease in other regions (from − 1.03% [Doryteuthis opalescens] to − 15.04% decrease [Loligo reynaudii]). Increases in habitat suitability occurred mostly at higher latitudes (north of 50° N), while suitable habitat decrease was predicted for the tropical regions. These shifts in future habitat suitability were stronger under harsher emission scenarios. Starting in 2050 (with RCP scenarios 4.6, 6.0 and 8.5), as a result of warming of the Arctic, squid habitat may increase along both coasts of North America. In the Southern Hemisphere, squids may lose habitat with no poleward habitat alternatives to move into. Contrary to our hypothesis, these commercial squid do not stand to benefit from climate change. Since these squid are an important food source for marine megafauna and humans, it is imperative that climate change biogeographic impacts are considered for a sustainable management of this important group of molluscs.
Vanessa M. Lopes, Mélanie Court, Martim Costa Seco, Francisco O. Borges, Bernardo Vicente, Sandra Lage, Ana Catarina Braga, Bernardo Duarte, Catarina Frazão Santos, Ana Amorim,et al.
MDPI AG
Marine heatwaves (MHWs) have doubled in frequency since the 1980s and are projected to be exacerbated during this century. MHWs have been shown to trigger harmful algal blooms (HABs), with severe consequences to marine life and human populations. Within this context, this study aims to understand, for the first time, how MHWs impact key biological and toxicological parameters of the paralytic shellfish toxin (PST) producer Gymnodinium catenatum, a dinoflagellate inhabiting temperate and tropical coastal waters. Two MHW were simulated—category I (i.e., peak: 19.9 °C) and category IV (i.e., peak: 24.1 °C)—relative to the estimated baseline in the western coast of Portugal (18.5 °C). No significant changes in abundance, size, and photosynthetic efficiency were observed among treatments. On the other hand, chain-formation was significantly reduced under category IV MHW, as was PSP toxicity and production of some PST compounds. Overall, this suggests that G. catenatum may have a high tolerance to MHWs. Nevertheless, some sublethal effects may have occurred since chain-formation was affected, suggesting that these growth conditions may be sub-optimal for this population. Our study suggests that the increase in frequency, intensity, and duration of MHWs may lead to reduced severity of G. catenatum blooms.
Francisco O. Borges, Vanessa M. Lopes, Catarina Frazão Santos, Pedro Reis Costa, and Rui Rosa
MDPI AG
Harmful algal blooms (HABs) are considered one of the main risks for marine ecosystems and human health worldwide. Climate change is projected to induce significant changes in species geographic distribution, and, in this sense, it is paramount to accurately predict how it will affect toxin-producing microalgae. In this context, the present study was intended to project the potential biogeographical changes in habitat suitability and occurrence distribution of three key amnesic shellfish toxin (AST)—producing diatom species (i.e., Pseudo-nitzschia australis, P. seriata, and P. fraudulenta) under four different climate change scenarios (i.e., RCP-2.6, 4.5, 6.0, and 8.5) up to 2050 and 2100. For this purpose, we applied species distribution models (SDMs) using four abiotic predictors (i.e., sea surface temperature, salinity, current velocity, and bathymetry) in a MaxEnt framework. Overall, considerable contraction and potential extirpation were projected for all species at lower latitudes together with projected poleward expansions into higher latitudes, mainly in the northern hemisphere. The present study aims to contribute to the knowledge on the impacts of climate change on the biogeography of toxin-producing microalgae species while at the same time advising the correct environmental management of coastal habitats and ecosystems.
Francisco Oliveira Borges, Miguel Guerreiro, Catarina Pereira Santos, José Ricardo Paula, and Rui Rosa
Frontiers Media SA
IntroductionHistorically considered to be a single cosmopolitan species, the so called Octopus vulgaris species complex (OVSC) is now recognized to be a group of (at least) six cryptic species: O. americanus (in the west Atlantic), O. vulgaris (in the northeast Atlantic and Mediterranean Sea), O. aff. vulgaris (in the region of South Africa), O. tetricus (southeastern Oceania), O. sinensis (northwestern Pacific), and O. djinda (western Australia). The potentially different environmental preferences of this highly cryptic species complex may result in distinct consequences under future environmental conditions.MethodsThe present study employed species distribution models (SDM) using MaxEnt to investigate potential changes in habitat suitability and geographical distribution of the OVSC in the future (i.e., 2050, and 2100), across four representative concentration pathway scenarios (RCP-2.6, 4.5, 6.0, and 8.5, CMIP5).ResultsDifferential responses were observed in the OVSC species analyzed. Specifically, O. vulgaris and O. tetricus exhibited a severe loss in distribution across their predicted range; O. americanus exhibited projected extirpation close to the equator, with limited expansion towards the poles; O. aff. vulgaris was projected to lose half of its current distribution; O. sinensis exhibited moderate losses, with projected increases in northern areas; and finally, O. djinda exhibited limited losses to its distribution. Except for O. sinensis, increasing RCP severity exacerbated changes in mean habitat suitability and projected distribution gains and losses.DiscussionUltimately, this study provides information on the potential biogeographical effects of marine climate change on a key worldwide ecological and economic resource to further disentangle the effects over each OVSC species, with the goal of assisting toward the sustainable management of octopus species at the global scale.
H. Arthur Woods, Amy L. Moran, David Atkinson, Asta Audzijonyte, Michael Berenbrink, Francisco O. Borges, Karen G. Burnett, Louis E. Burnett, Christopher J. Coates, Rachel Collin,et al.
University of Chicago Press
Oxygen bioavailability is declining in aquatic systems worldwide as a result of climate change and other anthropogenic stressors. For aquatic organisms, the consequences are poorly known but are likely to reflect both direct effects of declining oxygen bioavailability and interactions between oxygen and other stressors, including two—warming and acidification—that have received substantial attention in recent decades and that typically accompany oxygen changes. Drawing on the collected papers in this symposium volume (“An Oxygen Perspective on Climate Change”), we outline the causes and consequences of declining oxygen bioavailability. First, we discuss the scope of natural and predicted anthropogenic changes in aquatic oxygen levels. Although modern organisms are the result of long evolutionary histories during which they were exposed to natural oxygen regimes, anthropogenic change is now exposing them to more extreme conditions and novel combinations of low oxygen with other stressors. Second, we identify behavioral and physiological mechanisms that underlie the interactive effects of oxygen with other stressors, and we assess the range of potential organismal responses to oxygen limitation that occur across levels of biological organization and over multiple timescales. We argue that metabolism and energetics provide a powerful and unifying framework for understanding organism-oxygen interactions. Third, we conclude by outlining a set of approaches for maximizing the effectiveness of future work, including focusing on long-term experiments using biologically realistic variation in experimental factors and taking truly cross-disciplinary and integrative approaches to understanding and predicting future effects.
Francisco O. Borges, Eduardo Sampaio, Catarina P. Santos, and Rui Rosa
University of Chicago Press
Global ocean O2 content has varied significantly across the eons, both shaping and being shaped by the evolutionary history of life on planet Earth. Indeed, past O2 fluctuations have been associated with major extinctions and the reorganization of marine biota. Moreover, its most recent iteration—now anthropogenically driven—represents one of the most prominent challenges for both marine ecosystems and human societies, with ocean deoxygenation being regarded as one of the main drivers of global biodiversity loss. Yet ocean deoxygenation has received far less attention than concurrent environmental variables of marine climate change, namely, ocean warming and acidification, particularly in the field of experimental marine ecology. Together with the lack of consistent criteria defining gradual and acute changes in O2 content, a general lack of multifactorial studies featuring all three drivers and their interactions prevents an adequate interpretation of the potential effects of extreme and gradual deoxygenation. We present a comprehensive overview of the interplay between O2 and marine life across space and time and discuss the current knowledge gaps and future steps for deoxygenation research. This work may also contribute to the ongoing call for an integrative perspective on the combined effects of these three drivers of change for marine organisms and ecosystems worldwide.
Francisco Borges, Vanessa Lopes, Ana Amorim, Catarina Santos, Pedro Costa, and Rui Rosa
Toxin-producing microalgae present a significant environmental risk for ecosystems and human societies when they reach concentrations that affect other aquatic organisms or human health. Harmful algal blooms (HAB) have been linked to mass wildlife die-offs and human food poisoning episodes, and climate change has the potential to alter the frequency, magnitude, and geographical extent of such events. Thus, a framework of species distribution models (SDMs), employing MaxEnt modeling, was used to project changes in habitat suitability and distribution of three key paralytic shellfish toxin (PST)-producing dinoflagellate species (i.e., Alexandrium catenella, A. minutum, and Gymnodinium catenatum), up to 2050 and 2100, across four representative concentration pathway scenarios (RCP-2.6, 4.5, 6.0, and 8.5; CMIP5). Despite slightly different responses at the regional level, the global habitat suitability has decreased for all the species, leading to an overall contraction in their tropical and sub-tropical ranges, while considerable expansions are projected in higher latitudes, particularly in the Northern Hemisphere, suggesting poleward distributional shifts. Such trends were exacerbated with increasing RCP severity. Yet, further research is required, with a greater assemblage of environmental predictors and improved occurrence datasets, to gain a more holistic understanding of the potential impacts of climate change on PST-producing species.
Catarina Pereira Santos, Eduardo Sampaio, Beatriz P. Pereira, Maria Rita Pegado, Francisco O. Borges, Carolyn R. Wheeler, Ian A. Bouyoucos, Jodie L. Rummer, Catarina Frazão Santos, and Rui Rosa
Frontiers Media SA
Despite the long evolutionary history of this group, the challenges brought by the Anthropocene have been inflicting an extensive pressure over sharks and their relatives. Overexploitation has been driving a worldwide decline in elasmobranch populations, and rapid environmental change, triggered by anthropogenic activities, may further test this group's resilience. In this context, we searched the literature for peer-reviewed studies featuring a sustained (>24 h) and controlled exposure of elasmobranch species to warming, acidification, and/or deoxygenation: three of the most pressing symptoms of change in the ocean. In a standardized comparative framework, we conducted an array of mixed-model meta-analyses (based on 368 control-treatment contrasts from 53 studies) to evaluate the effects of these factors and their combination as experimental treatments. We further compared these effects across different attributes (lineages, climates, lifestyles, reproductive modes, and life stages) and assessed the direction of impact over a comprehensive set of biological responses (survival, development, growth, aerobic metabolism, anaerobic metabolism, oxygen transport, feeding, behavior, acid-base status, thermal tolerance, hypoxia tolerance, and cell stress). Based on the present findings, warming appears as the most influential factor, with clear directional effects, namely decreasing development time and increasing aerobic metabolism, feeding, and thermal tolerance. While warming influence was pervasive across attributes, acidification effects appear to be more context-specific, with no perceivable directional trends across biological responses apart from the necessary to achieve acid-base balance. Meanwhile, despite its potential for steep impacts, deoxygenation has been the most neglected factor, with data paucity ultimately precluding sound conclusions. Likewise, the implementation of multi-factor treatments has been mostly restricted to the combination of warming and acidification, with effects approximately matching those of warming. Despite considerable progress over recent years, research regarding the impact of these drivers on elasmobranchs lags behind other taxa, with more research required to disentangle many of the observed effects. Given the current levels of extinction risk and the quick pace of global change, it is further crucial that we integrate the knowledge accumulated through different scientific approaches into a holistic perspective to better understand how this group may fare in a changing ocean.
Francisco O. Borges, Catarina P. Santos, José R. Paula, Enrique Mateos-Naranjo, Susana Redondo-Gomez, Janine Barbara Adams, Isabel Caçador, Vanessa F. Fonseca, Patrick Reis-Santos, Bernardo Duarte,et al.
Frontiers Media SA
Coastal areas host some of the planet’s most productive ecosystems, providing life-sustaining ecological services and several benefits to humankind, while also being some of the most threatened areas (e.g., by globalization, climate change, and biological invasion). Salt marshes are coastal habitats with a key role in food and shelter provisioning, sediment deposition, nutrient cycling and carbon storage. Spartina spp. is a genus of grass halophytes which occurs in salt marshes worldwide, and includes species with different invasive potential. We evaluated the effect of climate change in the distribution and invasion potential of five Spartina species (S. anglica, S. alterniflora, S. densiflora, S. patens, and S. maritima) at a global scale. Species distribution models (SDMs) were applied on species occurrence data and atmospheric environmental predictors (WorldClim 2.1) to project potential changes in habitat suitability and associated changes in distribution and species co-occurrence until the end of the century, across four Shared Socioeconomic Pathway scenarios (i.e., SSP1-2.6 to SSP5-8.5). Projections showed a global trend for increasing species co-occurrence, with a general range expansion potentiated by increasing pathway severity. This study suggests that Spartina species can potentially benefit from climate change, predicting poleward expansions in the Northern Hemisphere for most species, with results pointing at increased conflict and invasion potential in Northern Europe and East Asian shorelines, already under strong invasive pressure. S. anglica is projected to remain a successful invader, with more severe scenarios likely favoring greater expansions. S. alterniflora exhibits very low expansion comparatively, despite exhibiting the same northward distribution shift. SSP1-2.6 produced the smallest change to species co-occurrence, suggesting a smaller potential for invasion-related conflicts, although still registering a potential net expansion for the Genus. Despite their limitations, SDMs can help establish general trends in climate change ecology and inform policymakers and environmental agents to ensure the correct management of these habitats and, ultimately, ecosystems.
Joana Castro, Francisco O. Borges, André Cid, Marina I. Laborde, Rui Rosa, and Heidi C. Pearson
MDPI AG
Unmanned Aerial Vehicles (UAVs), or drones, have recently emerged as a relatively affordable and accessible method for studying wildlife. Vertical Take-off and Landing (VTOL) UAVs are appropriate for morphometric, behavioural, abundance and demographic studies of marine mammals, providing a stable, nonintrusive and highly manoeuvrable platform. Previous studies using VTOL UAVs have been conducted on various marine mammal species, but specific studies regarding behavioural responses to these devices are limited and scarce. The aim of this study was to evaluate the immediate behavioural responses of common (Delphinus delphis) and bottlenose (Tursiops truncatus) dolphins to a VTOL UAV flown at different altitudes. A multirotor (quadcopter) UAV with an attached GoPro camera was used. Once a dolphin group was located, the UAV was flown at a starting height of 50 m directly above the group, subsequently descending 5 m every 30 s until reaching 5 m. We assessed three behavioural responses to a VTOL UAV at different heights: (i) direction changes, (ii) swimming speed and (iii) diving. Responses by D. delphis (n = 15) and T. truncatus (n = 10) groups were analysed separately. There were no significant responses of T. truncatus to any of the studied variables. For D. delphis, however, there were statistically significant changes in direction when the UAV was flown at a height of 5 m. Our results indicate that UAVs do not induce immediate behavioural responses in common or bottlenose dolphins when flown at heights > 5 m, demonstrating that the use of VTOL UAVs to study dolphins has minimal impact on the animals. However, we advise the use of the precautionary principle when interpreting these results as characteristics of this study site (e.g., high whale-watching activity) may have habituated dolphins to anthropogenic disturbance.
Joana Castro, Ana Couto, Francisco O. Borges, André Cid, Marina I. Laborde, Heidi C. Pearson, and Rui Rosa
MDPI AG
Off mainland Portugal, the common dolphin (Delphinus delphis) is the most sighted cetacean, although information on this species is limited. The Atlantic coast of Southern Portugal is characterized by an intense wind-driven upwelling, creating ideal conditions for common dolphins. Using data collected aboard whale-watching boats (1929 sightings and 4548 h effort during 2010–2014), this study aims to understand the relationships between abundance rates (AR) of dolphins of different age classes (adults, juveniles, calves and newborns) and oceanographic [chlorophyll a (Chl-a) and sea surface temperature (SST)] variables. Over 70% of the groups contained immature animals. The AR of adults was negatively related with Chl-a, but not related to SST values. The AR of juveniles was positively related with SST. For calves and newborns, although the relationship between SST and AR is similar to that observed for juveniles, the effect could not be distinguished from zero. There was no relationship between Chl-a levels and the AR of juveniles, calves and newborns. These results corroborate previous findings that common dolphins tend to occur in highly productive areas demonstrating linkages between their abundance and oceanographic variables, and that this region may be a potential nursery ground.
Ana Rodrigues, Francisco O. Borges, Vasco Pissarra, Ana Luísa Maulvault, José R. Paula, Regina Bispo, and Rui Rosa
Springer Science and Business Media LLC
Ana Rita Lopes, Francisco Oliveira Borges, Cátia Figueiredo, Eduardo Sampaio, Mário Diniz, Rui Rosa, and Tiago Fernandes Grilo
Elsevier BV
Rui Rosa, Vasco Pissarra, Francisco O. Borges, José Xavier, Ian G. Gleadall, Alexey Golikov, Giambattista Bello, Liliane Morais, Fedor Lishchenko, Álvaro Roura,et al.
Frontiers Media SA
Francisco O. Borges, Catarina P. Santos, Eduardo Sampaio, Cátia Figueiredo, José Ricardo Paula, Carlos Antunes, Rui Rosa, and Tiago F. Grilo
The Royal Society
The dramatic decline of European eel ( Anguilla anguilla ) populations over recent decades has attracted considerable attention and concern. Furthermore, little is known about the sensitivity of the early stages of eels to projected future environmental change. Here, we investigated, for the first time, the potential combined effects of ocean warming (OW; Δ + 4°C; 18°C) and acidification (OA; Δ − 0.4 pH units) on the survival and migratory behaviour of A. anguilla glass eels, namely their preference towards riverine cues (freshwater and geosmin). Recently arrived individuals were exposed to isolated and combined OW and OA conditions for 100 days, adjusting for the salinity gradients associated with upstream migration. A two-choice test was used to investigate migratory activity and shifts in preference towards freshwater environments. While OW decreased survival and increased migratory activity, OA appears to hinder migratory response, reducing the preference for riverine cues. Our results suggest that future conditions could potentially favour an early settlement of glass eels, reducing the proportion of fully migratory individuals. Further research into the effects of climate change on eel migration and habitat selection is needed to implement efficient conservation plans for this critically endangered species.
Francisco O. Borges, Eduardo Sampaio, Cátia Figueiredo, Rui Rosa, and Tiago F. Grilo
Elsevier BV
Francisco O. Borges, Cátia Figueiredo, Eduardo Sampaio, Rui Rosa, and Tiago F. Grilo
Elsevier BV