Neuroethology in South America: past, present and future

Neuroethology seeks to understand the neural basis of natural behaviors. In contrast to classical behavioral neuroscience studies, which are carried out almost exclusively in a few laboratory species and with little interest in ecological adaptations, neuroethology examines a wide variety of species, frequently studying animals in their natural environments. It is driven by Krogh's principle: ‘For many problems there is an animal on which it can be most conveniently studied’ (Krebs, 1975). By investigating the physiology of behaviors of diverse animals in their natural habitats, neuroethologists aim to understand behavior in the context of ecological adaptations and evolution, and thus to assess whether findings are generalizable across taxa.

South America has a land area about three times that of Europe, with nearly half its human population. It is a continent of extremes. It has the world's longest and mightiest river (Amazon), the driest desert (Atacama) and the highest mountain of the Americas (Aconcagua). The long latitudinal extent of South America contributes to its treasured diversity of biomes and species. Yet, its fauna remains poorly explored, making it a land of abundant opportunities for neuroethological research.

South America is also extreme in having the largest economic inequality of any continent in the world (Alvaredo and Gasparini, 2015). Furthermore, the status of scientific research among the 12 sovereign countries of the continent varies widely (Fig. 1A). Several South American countries have important scientific traditions, with universities established more than 400 years ago that offer long-standing PhD programs, whereas other countries have only recently developed a program of scientific research (Forero et al., 2020). Beyond these differences among countries, South American science faces common challenges that have historically hindered its impact on international science (Silva et al., 2022). One of them has been the significant interruptions of democratic life, especially in the 1960s and the 1970s, when most countries were ruled by barbaric military dictatorships. Besides the horrors inflicted on the people by these governments, this caused a mass exile of the most capable scientists, producing a gap in the formation of young scientists that encompassed two generations. Democracy returned to most countries during the 1980s, bringing intellectual freedom and hence the renascence of South American science. Yet, political and economic instability continues to be a hallmark of the region. Nowadays, however, the most critical challenge is the limited funding for research, which compromises the development of South American science in multiple ways, from restricting the acquisition of reagents and equipment to rendering publication costs unaffordable. Scientists from the Southern Cone also have long travel distances to attend international meetings and to cultivate research collaborations.

Despite these limitations, South American researchers have produced high-quality original research, as attested, for example, by their many papers published in Journal of Experimental Biology (JEB) that have been cited frequently (e.g. Balbuena et al., 2015: 259 citations; Caputi et al., 1998: 149 citations; Oliva et al., 2007: 131 citations). Notably, these articles originated from South America-based researchers, and are not ‘parachute science’, i.e. studies led by researchers from developed countries who merely collect samples in South America (Harris, 2004). Here, we briefly describe the reasons and strategies that led to the current development of the field of neuroethology in the region, and discuss how we envision the future of the discipline.

The vitality of South American neuroethology is evident in its recent history, beginning with the meeting ‘Neuroethology of the Southern Cone’, held in Argentina 10 years ago. This meeting, which commemorated the work of Argentine neuroscientist Héctor Maldonado (1927–2010), resulted in a special issue of the Journal of Physiology Paris (Szczupak et al., 2014), with 16 contributions originating from neuroethology labs in South America. These studies encompassed the great diversity of topics and approaches in neuroethology and involved a wide variety of animals native to South America. This meeting was momentous for South American neuroethologists in gaining self-identity as a community of scientists. It was also the main antecedent of the International Congress of Neuroethology held in Montevideo, Uruguay, in 2016, which brought considerable global attention to South American neuroethology and is likely to have contributed to the increase in South American neuroethology studies published in JEB over the last decade (Fig. 1B).

The International Society for Neuroethology (ISN, https://neuroethology.org/) was formed in 1981, and it took more than 30 years for its biennial meeting to be held for the first time in the southern hemisphere. Although South American neuroethologists represent less than 5% of ISN membership, they attended the International Congress of Neuroethology (ICN) in Montevideo in 2016 in great numbers, contributing 25% of all its presentations (Fig. 1C). These numbers reflect the potential of the South American neuroethology community as well as the limitations that prevent this community from affording society memberships and international meetings. Interestingly, at the 2016 ICN, South American researchers presented work on more than 20 invertebrate and vertebrate native species (Fig. 1D), broadening the knowledge of South American biodiversity.

There is a long tradition of training in neuroethology in South America, which has resulted in significant dissemination of the discipline and expansion of the neuroethology community. For instance, at the University of Buenos Aires, Argentina, a course on behavioral neurobiology enrols around 30 students each year and has now been taught for more than three decades. Notably, several Latin American Graduate Schools of Neuroethology sponsored by the International Brain Research Organization, ISN and local agencies were organized during the last decade. Each school gathered 20 Latin American graduate students for 3 weeks of intensive training with leading scientists from the USA and Europe. Many of these trainees (more than 60 students from at least seven South American countries) are currently working in the field of neuroethology in South America and abroad.

Many South American neuroethologists have used traditional experimental models for their studies, i.e. non-native animals such as the honey bee and the fly Drosophila. Here, however, we aim to highlight the value of contributions made by studying non-traditional animal models native to South America. Indeed, we will focus on only two model systems, the weakly electric fish Gymnotus omarorum and the mudflat crab Neohelice granulata, which stand out for their long-standing contributions as iconic models of global neuroethology developed in autochthonous South American animal species (Fig. 1D). In making this choice, we acknowledge that further significant contributions have been made by numerous groups in South America studying both native and non-native species.

The weakly electric fish G. omarorum (Fig. 2A) owes its name to the two pioneering Uruguayan scientists who developed it as a neuroethological model. Omar Macadar and Omar Trujillo-Cenóz (Fig. 2B) were heavily influenced by Ted Bullock (University of California, San Diego), who was the father of the field of active electroreception (Bullock, 1999) and who encouraged ‘the Omars’ to collaborate and to explore the electric fish in Uruguay. We thus credit Bullock with the birth of the neuroethological model of electric fish in Uruguay, the fruitful collaboration between the Omars and the first identification of the habitat of the most abundant native electric fish in Uruguay.

Shortly after publishing the first Uruguayan paper on electric fish (Trujillo-Cenóz et al., 1984), the Omars began referring to this seminal work as the ‘Old Testament’, because it established the foundational anatomo-functional concepts that linked the innervation pattern of the electric organ in Gymnotus carapo (now known as omarorum) with the waveform of its electric discharge. Soon after, three complementary articles offered a comprehensive view of the structure–function coupling of the electrogenic system (Trujillo-Cenóz and Echague, 1989; Macadar et al., 1989; Caputi et al., 1989). These elegant studies used electron microscopy, intracellular electrophysiological recordings and biophysical measurements, all state-of-the-art techniques at the time, to reveal the complexity of the spatiotemporal discharge pattern of the electric organ of G. omarorum. This research not only contributed to the general understanding of the temporal precision of the nervous system, but it also put Uruguayan neuroethology on the world map. Since then, more than 120 papers unravelling different aspects of electrosensation and communication have been published by the team founded by the Omars. In particular, the Gymnotus model has subsequently been the subject of two additional lines of research: the neural coding of electrosensation and communication, and the neuroendocrine bases of social behavior. Angel Caputi, Ruben Budelli and their colleagues have applied a cognitive approach to understand the computations made by the brain to create and interpret electric images (Caputi et al., 1998; Budelli and Caputi, 2000). Gymnotus omarorum is also recognized as the best-understood teleost model for the study of neuroendocrine mechanisms of aggression uncoupled from reproduction (Silva et al., 2013; Quintana et al., 2021). The path embarked upon by the Omars was indeed expanded by the three generations of scientists who were trained under their influence and who keep their legacy alive (Fig. 2C).

The crab Neohelice (previously Chasmagnathus) granulata (Fig. 3A) is a burrowing semiterrestrial species inhabiting the intertidal zone of estuaries, salt marshes and mangroves of the Southwestern Atlantic Ocean. Despite its circumscribed regional distribution, N. granulata is one of the five most-studied crab species in the world. The use of this animal as a model system for studying behavioral neurobiology – in particular the neurobiology of learning and memory – was introduced in the mid-1980s by Héctor Maldonado when he returned to Argentina after 18 years of exile (Fig. 3B; Tomsic and Maldonado, 2014). Since then, more than 120 papers addressing different mechanistic aspects of behavior in this crab have been published by the team founded by Maldonado. These studies have employed a wide variety of methodologies, including behavioral analyses in the field and laboratory, interspecific comparisons, pharmacology, electrophysiology, neuroanatomy, imaging, molecular biology and modeling. The first identification of individual neurons supporting long-term visual memory in any arthropod was achieved in this animal (Tomsic et al., 2003). More generally, this crab (Neohelice) has become a widely recognized invertebrate model for investigating mechanisms of learning and memory, and these studies are well cited (e.g. Pedreira et al., 2004: 470 citations; Tomsic et al., 1998: 123 citations; Freudenthal and Romano, 2000: 145 citations). Studies on the crab have also contributed to our understanding of the neural control of visually guided behaviors, in particular the escape response to predator stimuli. In the past decade, JEB has published a series of papers documenting neurons in the crab's brain that respond to looming stimuli that mimic the approach of a predator (Oliva et al., 2007; Oliva and Tomsic, 2012, 2016). This work has inspired bioengineering research (e.g. Luan et al., 2021, 2023), and has made the crab an attractive model for investigating the visual control of behaviors. Additional studies in JEB have reported on the robust prey capture behavior displayed by this crab and have introduced the animal as a promising model for investigating decision-making processes and animal personality (Tomsic et al., 2017; Gancedo et al., 2020; Salido et al., 2023). Finally, studies on Neohelice have generated important insights into visual processing. For example, they provided the first representation of the whole visual field by neurons sensitive to object motion described in any arthropod (Medan et al., 2015).

Altogether, 40 years of research on Neohelice have generated the most thorough account of the neuroanatomy, cytoarchitecture and neuronal functions subserving visual behaviors that we have for any decapod crustacean (e.g. Tomsic, 2016; Tomsic and Sztarker, 2019). Much of this work has been possible because the crabs are locally abundant. This reduces the cost of capturing and maintaining the animals, which is an important consideration when doing research in a country with limited research funds. The fact that Héctor Maldonado chose a native species was crucial in establishing this important neuroethological model. His research on these crabs helped to launch neuroethology in Argentina and promote its recognition by the international community. Maldonado's direct disciples and second-generation disciples continue his legacy (Fig. 3C).

The globalization of science has had a very positive impact on South America. Open access to information, virtual networks and inclusion policies have brought South America closer to mainstream science and have reduced the isolation felt by South American scientists. However, new challenges have emerged that still hinder the worldwide recognition of South American scientific contributions, such as the costs of shipment and travel (which have increased hugely after the COVID-19 pandemic), and the high publication charges imposed by most international journals. When considering both the historical and current constraints faced by scientists in South America, the development of neuroethology in this region is remarkable, particularly in the Southern Cone. This is largely due to the dedication of scientists whom, during the 1980s, returned to their home countries and committed to developing the discipline through teaching and training, and to the fact that their disciples took up the mantle and continue to promote neuroethology by organizing regional schools and international meetings. The amplifying effect of these actions guarantees a healthy future for South American neuroethology in terms of human resources. Furthermore, the still largely unexplored regional biodiversity of the area offers wonderful research opportunities that will surely continue to engage both local scientists and those from abroad.