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Underground life

Adaptation to lightless environments gives rise to odd-looking fauna and unexpected resources

Padre Grotto in Bahia: 16 kilometers of rich, unexplored diversity

léo ramosPadre Grotto in Bahia: 16 kilometers of rich, unexplored diversityléo ramos

Crouching at the water’s edge or right in it, researchers from the Federal University of Lavras (UFLA), in Minas Gerais, search for one-half-centimeter-long invertebrates that resemble white shrimp. They scarcely notice the pilgrims filling plastic bottles with water—famed for its miraculous properties—and shouting “hallelujah” in praise of this small grotto in the municipality of Bom Jesus da Lapa in southwest Bahia. This is the very same water where these invertebrates survive amidst rusty cans and old batteries. Despite the bustle of human activity, the organisms that live here are still undergoing description, by a group headed by biologist Rodrigo Lopes Ferreira.

Rafaela Pereira, a doctoral candidate in biology working under the advisorship of Ferreira, is describing these tiny shrimp of the genus Spelaeogammarus as part of her dissertation. In July 2014, Pereira, with the assistance of her advisor and of intern Gabrielle Pacheco, used an aquarium net to collect samples from the waters of Milagres (miracles) Grotto. Back in the laboratory, Pereira will dissect each of these minute crustaceans of the order Amphipoda, measure their appendages, and thus be able to compare and characterize the various species.

Spelaeogammarus collected in Bom Jesus da Lapa (left), and Cave catfish from Goiás, at the UFSCar laboratory (bottom)

léo ramosSpelaeogammarus collected in Bom Jesus da Lapa (left), and cave catfish from Goiás, at the UFSCar laboratory (bottom)léo ramos

During the same expedition, the group from Minas also explored Padre Grotto, a hard-to-reach cave in the municipality of Santana, adjacent to Bom Jesus da Lapa; little research has been done at this sixteen-kilometer-long grotto, where a huge rock wall at the mouth leaves no doubt about the visitor’s insignificance. After passing through a series of large chambers, the research team had to sit in inner tubes to traverse a two-km-long stretch of water. “The passage is over 40 meters tall,” says Ferreira, amazed by what he saw there. Hours after entering the grotto, roughly halfway through their task, the group had to abort their expedition, but they still returned to the open air in possession of at least seven new species of invertebrates—a commonplace feat for cave investigators. “There hasn’t been much study in this region of Bahia, so virtually every small animal found here has yet to be described by science,” he explains. Back at Lavras, the collected specimens will be added to a list of those awaiting analysis and description.

It’s no wonder the bulk of Brazilian cave fauna remains unknown; speleobiology, or the study of cave life, is fairly new to Brazil. In 1974, when Eleonora Trajano began her undergraduate work in biological sciences at the University of São Paulo (USP), she never imagined she would one day be a pioneer in Brazilian speleobiology and would spend her career researching a realm immersed in darkness. Early on in college life, she joined the University Explorers Center in search of adventure and there found her passion. “The first comprehensive list of cave fauna was compiled by five biologists from the University Explorers Center in the 1980s,” the researcher says. Prior to that, a good share of the discoveries had been made by Europeans.

The UFLA team takes inner tubes to cross certain stretches of Padre Grotto

léo ramosThe UFLA team takes inner tubes to cross certain stretches of Padre Grottoléo ramos

According to Trajano, in those early days the collected animals were actually described by zoologists who had never set foot in a cave. The first extensive study in Brazil was done by the geneticist Crodowaldo Pavan, who later gained renown for his research on the fruit fly. Pavan conducted a genetic analysis of Pimelodella kronei (a species of catfish endemic to Brazil) in the caverns of Iporanga, in Ribeira Valley, southern São Paulo State. In his dissertation, defended in 1944 and considered the first Brazilian investigation of the evolutionary genetics of animals, the scientist asserted that this fish, discovered half a century earlier by German-born Ricardo Krone, was not a species distinct from the one inhabiting the rivers outside the cave. Trajano explains that this blind catfish is a newer troglobite, that is, an animal that dwells in the dark parts of caves; it displays large within-species variations in coloring (ranging from white to heavily pigmented) and in regression of the eyes—generally so small that they are not always visible externally.

Trajano did her master’s on bats, who spend part of their time in caves but make daily forays outdoors in search of food; she then strengthened her academic ties to underground fauna by selecting the species Pimelodella kronei for her dissertation topic. By comparing the ecology, behavior, and morphology of this fish and its closest relative, P. transitoria, which is not necessarily a cave-dweller, Trajano concluded that the research conducted in the 1970s by Guy Collet, of France, left behind a negative mark. “He installed a laboratory inside the cave and made a complete mess of things,” she states. By plotting growth curves for the 1980s, she ascertained that the population of fish born in 1970 had suffered a drastic reduction; mortality had in fact been so severe that an entire generation was all but eliminated. “It took 25 years for the population to begin recovering,” she says, based on information drawn from the master’s thesis defended in 2011 by Ana Luiza Guil, who set out to repeat her advisor’s doctorate. In 2012, Trajano retired from the USP Biosciences Institute, where she still serves as senior professor. Many of these results depend on mark-recapture experiments that accompany populations over many years.

Bom Jesus da Lapa shrine has been drawing crowds since the 17th century

léo ramosBom Jesus da Lapa shrine has been drawing crowds since the 17th centuryléo ramos

Another world
These white fish with miniscule eyes—or no eyes at all—are so peculiar that they appear almost fictional. And they are no exception among cave creatures. In the May 2014 issue of Current Biology, Rodrigo Ferreira, along with colleagues from Japan and Switzerland, published a description of four fly-like insect species of the genus Neotrogla that measure less than four millimeters in length. The Lavras team had a surprise. Unable to identify the species, found in caverns in Minas, Tocantins, and Bahia, they sent samples off to Charles Lienhard, a Swiss expert on Psocoptera, the order to which the bugs belong. Taking a closer look, Lienhard realized that the females have an erectile organ similar to a penis while the males have a vagina-like cavity. During copulation, which lasts around 55 continuous hours, the females use the organ to transfer semen to a reservoir inside their own abdomen. “This is the first case of reversed sex organs in the entire animal kingdom,” says Ferreira.

When it comes to looks, the truly fascinating creatures are colorless and ghostly transparent; their bodies or appendages are usually long and their wings short. One curious representative is the palpigrade, an arachnid. The critter’s body, never longer than three millimeters, resembles that of an ant, but the bristles on its long jointed tail, known as a flagellum, bring to mind a baby bottle brush. In iron ore caves in Pará, the Lavras team found two such species, which constitute the first record of the genus Leptokoenenia ever discovered outside an intertidal environment, according to an article published in PLOS One in 2013 as part of the doctoral work of biologist Maysa Villela Souza. A serious concern, however, is that these caves carved out in iron are threatened by mining operations. The environments are richer in fauna precisely because their geological properties prompt the formation of myriad small canals where tiny animals can dwell, as suggested in a paper by Marconi Souza Silva, published in Biodiversity and Conservation in 2011. Understanding the conditions under which the ancestors of these species established themselves in caves requires more in-depth research—a challenge for evolutionary studies of cave fauna but a potential goldmine as well.

Pilgrims collect water at Milagres Grotto

léo ramosPilgrims collect water at Milagres Grottoléo ramos

Another group that has made valuable contributions is led by biologist Maria Elina Bichuette, who in 2006 founded the Laboratory of Subterranean Research at the Federal University of São Carlos (UFSCar). Successor of the pioneering Trajano, her graduate advisor, Bichuette is passionate about cave fish, though she doesn’t overlook other animals as well, like snails of the genus Potamolithus, the subject of her master’s degree. In her travels through underground Brazil, Bichuette discovered the first troglobitic crab, the first cavernicolous sponge in South America, cave-dwelling amphibian isopods in the semiarid region of Brazil, and much more, financed largely by FAPESP.

Jonas Gallão, a doctoral candidate at the laboratory, focuses his studies on cavernicolous scorpions. Found in Bahian caves, troglorhopalurus translucidus is the only known troglobitic species of this arachnid in Brazil. With reduced eyes and pedipalps (a kind of tactile foot) longer than those of non-cave scorpions, it seems well adapted to its environment. Gallão suspects that the lesser-differentiated Rhopalurus lacrau scorpion, which has never been recorded outside a cavern, may inhabit this environment and no other. He has tested mating in the laboratory and plans to analyze the potency of both species’ venom. He’ll leave aggression testing for last. “They’re cannibals,” he explains. “They’re top predators in the cave; they don’t let anything get by them.” He will also take body measurements using a technique known as geometric morphometrics and compare this scorpion with species that live near the examined caves. “Geometric morphometrics reveals subtle differences in animal forms that may be associated with the colonization of confined spaces and may include the isolation of sub-populations, data that are fundamental for conservation measures,” Bichuette explains.

The pigmented catfish Glaphyropoma spinosum exists only in the Diamantina Plateau

léo ramosThe pigmented catfish Glaphyropoma spinosum exists only in the Diamantina Plateauléo ramos

Doctoral candidate Camile Fernandes is studying relatives of the woodlouse, those tiny insects that roll themselves up into balls no more than 0.5 centimeters in diameter. These crustaceans from the order Isopoda are white or grayish in color and come in a variety of shapes when found in caves. Some protect themselves by curling up, others flatten themselves out to escape danger, and still others have bristled bodies that allow them to bury themselves without having grains of dirt stick to them. The speedier of the species have skinny bodies and long legs and can quickly flee predators. After collecting specimens inside and outside some 30 grottoes in Bahia and Goiás, Fernandes used each species’ morphological traits to conduct an ecological analysis known as functional diversity, unprecedented in the study of Brazilian subterranean fauna. “The idea was to test whether caves constitute an extreme environment for the animals that live inside them,” she explains. Contrary to what Fernandes expected to find given the lightless environment and generally scarce food supply, she concluded that woodlice do not suffer any greater selective pressure inside the caves than out. She had believed that intense natural selection would prompt the development of uniform characteristics but she found the opposite was true. “They are more diversified inside the subterranean environment than out, perhaps because there is greater variation in substrata and food resources inside the caves.” Alternatively, it may be that radical natural selection also occurs where they live on the surface.

Here is what’s remarkable: when the land is not very fertile, life has to be creative. And the basis for this creativity lies in the manifold environments found inside caverns. The wind and rains leave large amounts of organic matter near cave mouths. When heavier downfalls come, leaves and branches may travel far into their depths. And in areas where bats like to rest, where there is little or no light, guano—the excrement of these flying mammals—is more common.

The blind characid Stygichthys typhlops is notable for its specialization

léo ramosThe blind characid Stygichthys typhlops is notable for its specializationléo ramos

The UFLA team recently investigated the importance of guano as a food source. Thais Pellegrini, a doctoral student of Ferreira’s, examined deposits of guano in the Lapa Nova cave in northwest Minas Gerais. More than 157,000 individuals from 12 orders were found in a 15-by-5-meter patch of guano (divided into 25 20-cm2 sections for research purposes). Over 99% were mites, according to the article published in the European Journal of Soil Biology in 2013. Analysis showed that species richness varied with the amount of phosphorous and organic matter available and with soil moisture. As a result, species were more abundant in deposits of newer guano than in older. For reasons that are not yet clear, another area displaying great diversity was the interface of the guano patch with the adjacent soil.

Aquatic underworld
There’s water too. Caves are generally sculpted by it. Seeping out between cracks in the rocks, water dissolves some of their components; it flows into rivers and forms crystal-clear lakes. This is where Bichuette focuses much of her attention, spending long hours slowly snorkeling around to observe fish behavior, while taking notes in pencil on an underwater PVC board. Over the years, she has helped describe a number of blind catfish and other fish species, some of which she investigated in conjunction with Trajano. An example is Brazil’s strange blind characid (Stygichthys typhlops), one of the most extreme fish when it comes to modifying life to reside in a cave. Redescribed in 2010 in the Journal of Fish Biology, this 5-cm-long unpigmented characid has no eyes at all and inhabits caves in Minas Gerais, in the São Francisco River Basin; it is severely endangered because water from its home aquifer is often used to irrigate banana plantations.

020-029_cavernas_224A large part of the country’s underground fish diversity lies in Central Brazil, where the caverns contain very large amounts of water. One intriguing example is the Ituglanis epikarsticus pencil catfish, found in the region of São Domingos, in Goiás, where it inhabits waters that are hidden even from someone inside the cave. “This is the world’s only record of a vertebrate in the epikarst,” explains Bichuette, referring to the zone of rock beneath the surface where percolating water is detained; there it penetrates caves solely by dripping off the ceiling, often forming the famous adornments known as stalactites and stalagmites (see infographic). “A subterranean biologist has to have good spatial awareness,” the researcher says. “He has to know, or at least suspect, where the water comes from.” Accordingly, Bichuette believes it is crucial to partner with geologists and other speleologists.

After Bichuette’s interest in the epikarst zone had been spurred by the discovery of this fish, she conducted a broader study of the water in São Domingos. She collected dripping water in six caves and found 36 species of organisms invisible to the naked eye, according to an article published in 2013 in Systematic Biology. “Just because you can’t see it doesn’t mean it doesn’t matter.” Even though she gathered only a small amount of microscopic fauna in these droplets, it displayed great diversity and was often unique to its environment, as compared to the fauna detected in the waters of external rivers and in those flowing through caves.

Much as caves seem like a world apart, they are an extension of the outside world. As animals cope with the climate fluctuations and changes in plant life that transpire over the course of millennia, they can turn to these shelters where temperature and humidity are almost constant, even if the availability of resources there varies between alternating wet and dry periods. Once inside a cave, animal populations gradually specialize until forming distinct species. This explains why many subterranean species have close relatives living outside caves (except in cases where the ancestral species is extinct). Geologist Ivo Karmann, of the USP Geosciences Institute, does not find Brazil’s broad cavernicolous diversity surprising. “We have caves across a wide range of latitudes, from the tropical to the subtropical,” he says, pointing to a map. The combination of rock properties, climate variation, and variations in outside fauna according to biome could produce nothing but this result.

The legs of an amblypygid make it look like something out of a horror film

léo ramosThe legs of an amblypygid make it look like something out of a horror filmléo ramos

During her post-doc, Bichuette analyzed five populations of the blind catfish Rhamdiopsis krugi of the Diamantina Plateau and compared them with a species that inhabits a nearby outside river. The results were published in an article co-authored by Trajano, Bianca Rantin (UFSCar), and Erika Hingst-Zaher (Butantan Institute) and recently accepted for publication in the Biological Journal of the Linnean Society. Using geometric morphometrics—which has proven as valuable as genetics in research on the evolution and possible colonization of underground habitats by the catfish—these researchers have shown that there is differentiation between the populations of the two basins where the caves are located, in Irecê and Una/Utinga. Conjoining geology and biology, scientists postulate that these lineages have been isolated for at least ten million years, when the last link between the two basins closed. “The variations in the forms of these catfish reflect the separation of the basins,” says Bichuette, who feels that measures must be taken to protect both lineages.

In analyzing the data on these different catfish populations, Trajano devised a two-step model of colonization to account for what the scientists saw. Starting as fish in an aboveground river, the species gradually explored spaces in the sediment beneath the riverbed. The smaller ones established themselves in this environment, occupying increasingly smaller fissures. The result was the miniaturization observed in some fish in the caves under study. Those that established themselves in larger bodies of water—like Poço Encantado, whose depth reaches 65 meters—sometimes developed new mechanisms of spatial orientation. Larger ones may enjoy an advantage under these conditions. The model applies to these fish, which are about two inches long, but does not hold for the nearly six-inch-long blind catfish of Iporanga, which Trajano researched at the outset of her career. “They must have entered through the mouth of the cave,” the USP scientist conjectures.

T. translucidus: the first cave scorpion ever recorded in Brazil

léo ramosT. translucidus: the first cave scorpion ever recorded in Brazilléo ramos

Endangered
The experts are all aware of the risk of losing these worlds that are home to deep lakes, naturally canalized rivers, aragonite crystals, awe-inspiring chambers, and exceedingly odd fauna. In 2008, a Brazilian decree-law did away with the integral protection formerly accorded caves and put in effect measures to offset destruction based on the relevance of each cave. “Uniqueness earns top relevance; if everything is redundant, there’s no problem,” Trajano concedes. But no major studies are a prerequisite to obtaining permission to mine ore, remove water, or engage in any other type of destructive exploitation. “Consultation with experts was not taken into consideration at the most critical points,” she says.

Brazilian law stipulates that only two expeditions are necessary to ascertain whether a cave is a site of animal treasures. The problem is that this does not suffice. “Sometimes it’s four or five visits before we stop finding new things,” says Bichuette. What’s worse is that the two required visits are not replications, since one takes place during the dry season and the other during the wet, when distinct conditions may mean that the fauna is likewise distinct. In Trajano’s view, an adequate assessment requires three years of work, which is never the case.

Tiny pseudoscorpions hide in nooks and crannies

léo ramosTiny pseudoscorpions hide in nooks and cranniesléo ramos

In addition to destructive exploitation, another worry is cave tourism. Trajano and Bichuette were co-authors of a study led by Heros Lobo, of UFSCar’s Department of Geography, Tourism, and the Humanities, which analyzed the visitor-carrying capacity of tourist caves like Diabo, in southern São Paulo State. Published in 2013 in Tourism Management, the article proposes a formula for calculating how many visitors can enter a cave per day, taking into account maps of fragile areas. The installation of suspended walkways and other resources may help avert greater damage, although the construction process itself can be harmful.

Architect Marcos Silverio, who is doing his master’s degree at the USP School of Architecture and Urban Studies and using Diabo Cave as a case study, proposes ways of balancing preservation concerns with human use. Silverio fell in love with speleology long before becoming an architect. “As a more rudimentary expression of the essence of architecture, caves were man’s first shelter and are symbolic places, which, ever since pre-history, have sparked human curiosity and the thirst for adventure, mystery, and beauty,” he says. Despite all the protective structures that have been built, he warns that damage is still concentrated in the tourist stretch because Diabo has so many visitors per year. The cave’s waters harbor a small species of the crustacean Aegla strinatii that exists in no other region. In the architect’s opinion, environmental studies are indispensable to defining protection. For instance, it is essential to know whether an animal is more vulnerable during the mating season and how to minimize damage.

Harvest spiders use their elongated appendages much like the blind use canes

léo ramosHarvest spiders use their elongated appendages much like the blind use canesléo ramos

According to Silverio, many management plans are poorly designed. One current legal restriction, for example, is that no impact can occur within a radius of 250 meters from a cave. “But how do you measure this distance?” he asks. It’s not enough to take the mouth into account while overlooking underground galleries. Everything has to be taken into consideration: the material used for visitor structures cannot release contaminants or be propitious to microorganisms; pathways must be demarcated; and there must be a minimal number of carefully thought-out structures. An architect’s delight.

Bom Jesus da Lapa shrine is an example of how caves stir something religious even in non-believers. Erected inside a grotto discovered at the close of the 17th century, the spot draws thousands of pilgrims every August. Beyond the sanctuary, a series of chambers holds countless offerings: wooden and wax models of arms, legs, and even babies; miniature houses, sometimes alongside the owner’s photo; and pictures and notes stuck into cracks in the rock. Even scientists may not be able to resist a feeling of reverence. In many cases, this is precisely part of what led them to study this environment.

Projects
1. Brazilian subterranean aquatic fauna: biodiversity, biology, evolution, ecology, and conservation (2003/00794-5); Principal investigator Eleonora Trajano (USP); Grant mechanism Thematic Project; Investment R$ 518,889.68 (FAPESP).
2. Are the São Desidério, Serra do Ramalho (southwest Bahia) and São Domingos (northeast Goiás) biodiversity hot spots karstic areas? Cave community analysis and protection criteria (2010/08459-4); Principal investigator Maria Elina Bichuette (UFSCar); Grant mechanism Regular Line of Research Project Award; Investment R$ 146,201.14 (FAPESP).

Scientific articles
BICHUETTE, M.E. et al. Geometric morphometrics throws light on evolution of the subterranean catfish Rhamdiopsis krugi (Teleostei: Siluriformes: Heptapteridae) in eastern Brazil. Biological Journal of the Linnean Society. In press.
SIMÕES, L.B. et al. Aquatic biota of different karst habitats in epigean and subterranean systems of Central Brazil – visibility versus relevance of taxa. Subterranean Biology. V. 11, pp. 55-74. 2013.
YOSHIZAWA, K. et al. Female penis, male vagina, and their correlated evolution in a cave insect. Current Biology. V. 24, No. 9, pp. 1006-10. May 5, 2014.

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