Marine and coastal biodiversity studies, 60 years of research funding from FAPESP, what we have learned and future challenges / Estudos de biodiversidade marinha e costeira, 60 anos de financiamento à pesquisa da FAPESP, o que aprendemos e desafios futuros

Abstract In this study we survey and analyze 300 projects related to marine biodiversity funded by FAPESP from 1972 to 2021, of which 46 were nested in the BIOTA Program. From a unique project in the 1970's, the number gradually increased until 2009, when BIOTA promoted a call on marine biodiversity, which led to a boost in the number of funded projects in the subsequent years. The geographical range of the projects expanded over the years and, from studies based on the coast of São Paulo State, the focus gradually shifted to broader areas of the Brazilian coast, then to other areas of the Atlantic, and eventually became global. The majority of projects focused on coastal benthic organisms living on hard-bottom. In terms of taxa, six groups accounted for about 60% of the projects (viz. Crustacea, Actinopterygii, Mollusca, Chondrichthyes, Cnidaria, and Rhodophyta), but it is observed an increase in the number of groups studied over the decades. The 300 projects refer to a set of 82 different topics, of which the top five are taxonomy, phylogeny, community, "omics", and pollution. The analyses show a long-standing effort in marine biodiversity surveys, with ongoing updated approaches regarding scope and methods. Research on strategic areas is discussed, including deep-sea and marine microbiota. Climate change and the increasing pressure of human activity on the ocean, including pollution, acidification and invasive species, are among the main challenges for the future. Projects producing and using basic research data in an integrative and transdisciplinary way offer multiple perspectives in understanding changes in ecosystem functioning and, consequently, are essential to support public policies for the conservation and sustainable use of marine biodiversity at different scales. UNESCO's Decade of Ocean (starting 2021) is a window of opportunity to strengthen marine research, to promote national and international collaboration, to build up networks involving the public and private sector, but particularly to draw society's attention to the importance of knowing marine environments and using ocean resources in a sustainable way. The advancement of ocean literacy is one of the main legacies for future generations promoted by integrated research programs such as BIOTA-FAPESP.

Resumo Neste estudo levantamos e analisamos 300 projetos relacionados à biodiversidade marinha financiados pela FAPESP entre 1972 a 2021, dos quais 46 foram realizados no Programa BIOTA. De um projeto único na década de 1970, o número foi aumentando gradativamente até 2009, quando o BIOTA promoveu uma chamada sobre biodiversidade marinha, o que impulsionou o número de projetos financiados nos anos seguintes. A abrangência geográfica dos projetos se expandiu ao longo dos anos e, a partir de estudos baseados no litoral do Estado de São Paulo, o foco gradualmente se deslocou para áreas mais amplas da costa brasileira, depois para outras áreas do Atlântico, e acabou se tornando global. A maioria dos projetos se concentrou em organismos costeiros, bentônicos, em substrato consolidado. Em termos de táxons, seis grupos responderam por cerca de 60% dos projetos (Crustacea, Actinopterygii, Mollusca, Chondrichthyes, Cnidaria e Rhodophyta), mas observa-se um aumento no número de grupos estudados ao longo das décadas. Os 300 projetos referem-se a um conjunto de 82 temas diferentes, dos quais os cinco principais são taxonomia, filogenia, comunidade, "ômicas" e poluição. As análises mostram um esforço de longa data em pesquisas de biodiversidade marinha, com abordagens atualizadas em relação ao escopo e métodos. A pesquisa em áreas estratégicas é discutida, incluindo os estudos sobre a microbiota marinha e em águas profundas. As mudanças climáticas e a crescente pressão da atividade humana sobre o oceano, incluindo poluição, acidificação e espécies invasoras, estão entre os principais desafios para o futuro. Projetos de produção e uso de dados de pesquisa básica de forma integrada e transdisciplinar oferecem múltiplas perspectivas de compreensão das mudanças no funcionamento dos ecossistemas e, consequentemente, são essenciais para subsidiar políticas públicas de conservação e uso sustentável da biodiversidade marinha em diferentes escalas. A Década do Oceano da UNESCO (a partir de 2021) é uma janela de oportunidade para fortalecer a pesquisa marinha, promover a colaboração nacional e internacional, construir redes envolvendo os setores público e privado, mas principalmente para chamar a atenção da sociedade para a importância de conhecer os ambientes marinhos e utilizar os recursos oceânicos de forma sustentável. O avanço da "alfabetização" oceânica é um dos principais legados para as gerações futuras promovidos por programas integrados de pesquisa como o BIOTA-FAPESP.

Losers can win: Thermoregulatory advantages of regenerated claws of fiddler crab males for establishment in warmer microhabitats.

Fiddler crab males present a hypertrophied claw, which is used for sexual and aggressive displays, fights with competitors, and has been proposed as an important thermoregulatory organ for heat control. Two claw morphologies can be observed within fiddler crab populations: brachychelous claws (unregenerated) and leptochelous claws (regenerated). The leptochelous morphotype presents less muscle mass and longer fingers, resulting in a less advantageous weapon in fights. Considering their slender shape, we hypothesized that the leptochelous morphotype would present lower thermal inertia and be more efficient at body heat dissipation. We evaluated the role of the fiddler crabs' claw shape as a heat sink and how this influences their distribution between unshaded and shaded microhabitats. We tested in the field whether the proportion of adult male Leptuca uruguayensis with leptochelous claws was higher in unshaded microhabitats than shaded ones. In the laboratory, we tested if heat transfer between the body and claw is higher in leptochelous males than in brachychelous males. Spontaneous waving behaviour and active time above the surface were compared between both morphotypes in the field during the hottest period of the day. Leptuca uruguayensis with regenerated claws comprised more than 60% of the sampled male population of unshaded microhabitats compared to 18% in shaded microhabitats. Leptochelous males showed a mean heat transfer between body to claw 35% higher than that observed for brachychelous males. During the hottest period of the day, brachychelous males waved approximately 28% more than leptochelous males. Moreover, brachychelous males spent less time under the sediment surface since the surface temperature increased, while activity of leptochelous males was not associated with a temperature increase. Therefore, regenerated claws may be advantageous for the establishment of L. uruguayensis males in warmer and unshaded microhabitats because they are more efficient for heat loss and allow crabs to cool down, spending less time waving. Our study shows the relevant context of winners and losers in the face of climate change and highlights the importance of morphological variations in thermoregulatory structures for the occupation of thermal niches.

Intruder traits modulate aggressive behavior of territory owners.

The prior residence effect consists of a higher probability of territory owners to win a fight against intruders, as observed in several territorial species across animal kingdom. However, in investigations on territorial behavior, intruder traits have been assumed as fixed. Thus, we used a territorial species as experimental model to evaluate the effect of intruder traits on aggressive behavior of territory owners. During fights staged between territory owners and intruders, intruder traits, linked with visual signals of social status (dominant-subordinate position), modulate fighting behavior of territory owners, but prior residence effect still occurred. Intruder traits must be addressed more effectively for improving the theoretical understanding of territoriality.

Effects of temperature increase on the physiology and behavior of fiddler crabs.

Intertidal organisms rely on physiological and behavioral adjustments to maintain homeostasis under warm exposure. We examined the effects of the temperature increase related to climate warming on the physiology and behavior of two fiddler crab species: Leptuca uruguayensis, which inhabits mostly vegetated areas, and Leptuca leptodactyla, that inhabits unvegetated areas. We hypothesized that L. uruguayensis would be more sensitive to warming than L. leptodactyla. Crabs were exposed to different temperatures: 27 °C (control), 31 and 33 °C (+4 and +6 °C, respectively) for 15 days to evaluate their physiological responses (oxygen consumption, Q10, ammonia excretion and hepatosomatic index) and for 2 days to observe their behavioral responses (feeding rate and duration of burrow retreat). We also tested in situ the effect of air, surface, and body temperatures on the claw-waving display of both species. We found that species were affected differently by increasing temperature. Leptuca uruguayensis showed adaptation limit (Q10 <1), increasing oxygen consumption. Also, in comparison with control, L. uruguayensis decreased the ammonia excretion at 31 °C, but not at 33 °C, indicating a compensatory mechanism to cope with thermal stress. In contrast, L. leptodactyla was able to adjust its metabolic rate to temperature rise (Q10 ~3) and reduce ammonia excretion, suggesting changes in the energetic substrate and amino acid catabolism. Higher temperatures reduce the hepatosomatic index of both species, indicating increased use of energy reserve (although only the L. uruguayensis feeding rate was reduced). Furthermore, warmer temperatures increase the duration of burrow retreat in both species, potentially impacting social interactions, such as mating. Temperature increase did not affect the claw-waving display frequency, suggesting that other factors may affect this behavior, e.g., the presence of females and competitors. Specific behavioral (e.g., microhabitat selection) and morphological attributes (e.g., larger major claw) might benefit the thermoregulation of each crab species since no differences in body temperature were found between them in situ. Therefore, fiddler crabs that inhabit vegetated areas are more vulnerable to higher temperatures and may change its geographic range as a result of climate warming, while fiddler crabs that inhabit unvegetated areas are more tolerant to temperature rise and may have a competitive advantage under a temperature increase scenario.

Combined effects of predator odor and alarm substance on behavioral and physiological responses of the pearl cichlid.

Several fish species trigger defensive behavioral responses when exposed to chemical cues that indicate predation risk. In these situations, physiological adjustments are also necessary to prepare the organism for a defensive response and increase survival odds. Chemical cues may be derived from predator odor or injured conspecifics. However, little is known about the effects of both cues combined. Therefore, our study evaluated the combined effects of predator odor (PO) and conspecific alarm substance (CAS) on the anti-predatory responses of the pearl cichlid (Geophagus brasiliensis). We set 4 experimental conditions 1) PO + CAS; 2) PO + Distilled Water (DW); 3) DW + CAS; and 4) DW + DW (negative control). Fish exposed to DW + CAS had values of ventilation rate and feeding latency significantly higher than when exposed to the other conditions, which yielded similar responses for both variables. Our data show that the combination of PO + CAS interfered with pearl cichlid behavior and physiology since it abolished CAS defensive responses. These results show that CAS plays an important role on the defensive responses of pearl cichlids, while PO does not, given that fish did not respond to PO by itself. Our findings point to different cue-specific strategies in pearl cichlids when dealing with different chemical cues that indicate predation risk.

Differential effects of water loss and temperature increase on the physiology of fiddler crabs from distinct habitats.

Temperature is one of the main environmental constraints to organism distribution, affecting physiology and survival. Organisms that inhabit the intertidal zone are exposed to temperature variation and, with climate change, they should face different conditions which include higher temperatures, leading to higher rates of water loss through evaporation and then fitness reduction or mortality. Here we tested the effects of desiccation and increased temperature in two fiddler crabs species that occupy distinct habitats in regard to vegetation cover and position on the intertidal zone and thus may respond differently to these stressors. Leptuca thayeri, which is restricted to the mid-tide zone and vegetated areas, had higher desiccation and mortality rates than Minuca rapax, a generalist species, when exposed to desiccation for 120 min. Also, compared to M. rapax, L. thayeri had a more permeable carapace. Temperature elevation of 10 °C and 20 °C for 72 h caused no mortality in either species. However, there were changes in hemolymph osmolality and muscle hydration in both species. Leptuca thayeri osmolality was low in the intermediate temperature, suggesting that at this temperature this species has a better salt secretion capability. Minuca rapax, however, had an increase in hemolymph osmolality at the highest temperatures with no LDH increase, which indicates that osmotic control in this species is more sensitive to temperature increase. Our results show that L. thayeri suffers more from desiccation, due to a more permeable carapace. However, because of this higher permeability L. thayeri is capable of lowering its temperature more than M. rapax. As temperature elevation produces great physiological changes in M. rapax, a reduced ability to keep a low temperature can be an issue for this species if temperature increases. However, higher water loss to keep body temperature low may decrease L. thayeri survivability in the same scenario.

Chemical Profile of the Sulphated Saponins from the Starfish Luidia senegalensis Collected as by-Catch Fauna in Brazilian Coast.

The by-catch fauna of the shrimp fishery includes a number of marine invertebrates that are discarded because they do not have commercial value. In order to try to add some value to these materials, we analyzed the chemical composition of the starfish Luidia senegalensis collected in the Brazilian coast as a consequence of the trawling fishery method. In order to access their chemical composition, we used a combination of solid phase extraction (SPE) followed by ultra-high performance liquid chromatography coupled to electrospray ionization ion trap tandem mass spectrometry (UPLC-ESI-IT-MSn). Luidia senegalensis contains asterosaponins, which are sulphated glycosilated steroids, containing five and six sugar moieties, in addition to polyhydroxysteroids. This study helped us to support the presence of important and potentially bioactive compounds in invertebrates associated to the by-catch fauna of the shrimp fishery, using a fast and efficient method.

Aggressiveness overcomes body-size effects in fights staged between invasive and native fish species with overlapping niches.

Approximately 50 years ago, Nile tilapia were accidentally introduced to Brazil, and the decline of pearl cichlid populations, which has been intensified by habitat degradation, in some locations has been associated with the presence of Nile tilapia. There is, however, little strong empirical evidence for the negative interaction of non-native fish populations with native fish populations; such evidence would indicate a potential behavioural mechanism that could cause the population of the native fish to decline. In this study, we show that in fights staged between pairs of Nile tilapia and pearl cichlids of differing body size, the Nile tilapia were more aggressive than the pearl cichlid. Because this effect prevailed over body-size effects, the pearl cichlids were at a disadvantage. The niche overlap between the Nile tilapia and the pearl cichlid in nature, and the competitive advantage shown by the Nile tilapia in this study potentially represent one of several possible results of the negative interactions imposed by an invasive species. These negative effects may reduce population viability of the native species and cause competitive exclusion.

Reproductive pattern comparison of Uca thayeri Rathbun, 1900 and U. uruguayensis Nobili, 1901 ( Crustacea, Decapoda, Ocypodidae )

Fêmeas ovígeras de U. thayeri e de U. uruguayensis foram utilizadas para se avaliar e comparar o padrão reprodutivo. O tamanho médio das fêmeas foi de 6,6 ± 0,8mm para U. uruguayensis, variando de 17,3 ± 4,4mm para U. thayeri. A fecundidade média obtida para U. uruguayensis foi 1883 ± 490 ovos (N = 27) e para U. thayeri de 31068 ± 11185 ovos (N = 31). As diferenças observadas no padrão reprodutivo de U. thayeri e U. uruguayensis sugerem estratégias adaptativas: U. thayeri apresenta uma reprodução sazonal, com atividade pronunciada de janeiro a março e alta fecundidade, enquanto U. uruguayensis reproduz-se continuamente, mas com proles menores.