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    Microbial storage and its implications for soil ecology

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    Pharmacological modulation of fish-induced depth selection in D. magna: the role of cholinergic and GABAergic signalling

    Phototactic behaviourThe optimization results of the proposed behavioural setup allowed the phototactic behaviour of the studied D. magna clone and the effects of FK treatment on this behaviour to be monitored and quantified. Furthermore, the effects of the FKs were evident only upon light exposure, were more apparent after a short (5 min) acclimation to light and were tightly regulated by the light intensity. The above-mentioned factors agree with previous studies, which found a marked positive phototactism of clone P132,8528 and that the effects of the FKs become consistent after 5 min of light exposure28. Moreover, it has also been reported that light intensity controls anti-predatory defences in Daphnia29.The effects of the pharmacological treatments were consistent for GABAergic and muscarinic cholinergic compounds across two or three identical non-consecutive experiments performed over more than one year. Consistency of the toxicological results and, in particular, of the behavioural responses should be compulsory in toxicological studies to increase the credibility and robustness of the findings30,31. Agonists of these two neurotransmitter receptors (DZP, PILO) and the antagonist of the GABA receptor (PICRO) affected the induction of the phototactic behavioural changes (i.e., interfered with fish recognition). The receptor agonists DZP and PILO counteracted the negative phototactism evoked by the FKs, whereas PICRO enhanced the effect of the FKs, increasing the negative phototactism. None of the three applied substances when applied alone induced anti-predatory fish phototactic behaviour, indicating that these compounds interfered with the FK sensorial pathway. Alternatively, the muscarinic cholinergic antagonist SCOP interfered with phototaxis itself, almost completely abolishing the positive phototactic behaviour of the studied clone under both control and FK conditions. This indicates that the muscarinic cholinergic signalling pathway could potentially be a major regulator of anti-predatory fish phototactic behaviour. In D. pulex and D. galeata, the formation of neck teeth or helmets in response to predatory kairomones released by invertebrate predators has been related to a series of biological reactions that involve kairomone perception and neuronal signals, which are converted into endocrine signals and subsequently induce changes in the expression of morphogenetic factors32,33. We previously showed that DZP, PILO, PICRO and SCOP were neuroactive in D. magna, affecting sensitization and/or habituation motile responses to repetitive light stimuli34; thus, it is likely that these compounds disrupted neurological signalling pathways related to the phototactism shifts caused by FK perception or to the phototaxis itself.Little is known about how phototaxis is neuronally coded. In D. pulex, both in silico and experimental works have shown that histaminergic neurons may mediate phototactic responses to UV irradiation12. By using histamine immunohistochemistry, the previous authors labelled putative photoreceptors in the compound eye and neuronal projections from these cells to the brain. The D. pulex genome also has a putative Drosophila orthologue of histidine decarboxylase (the rate-limiting biosynthetic enzyme for histamine), as well as two putative histamine-gated chloride channels (hclA and hclB orthologues). Exposure of D. magna to cimetidine, an H2 receptor antagonist known to block both hclA and hclB in D. melanogaster, inhibited the negative phototactic responses of these orthologues to UV irradiation. In another study, it was found that short-day photoperiods induced a significant increase in light-avoidance behaviours relative to controls and increased glutamate signalling, which is a critical pathway in arthropod light-avoidance behaviour35. It has also been reported that a group of serotonergic cells located in the protocerebrum probably control phototactic behaviour16. Notably, the perception of predatory kairomones and neuronal and cellular wiring is largely unknown in Daphnia2. For example, the receptors that detect invertebrate cues from Notonecta in D. longicephala were shown to be located on the first antennae, from which neurites extend into the deutocerebrum of the brain. However, key olfactory neuronal structures, such as olfactory glomeruli in the deutocerebrum, were not found2.Our results obtained for DZP, an agonist of the GABAA receptor, agree with those of Weiss et al.11, who found that co-exposure to FKs and exogenous GABA ameliorated life history changes to FKs in a D. pulex clone, whereas co-exposure with the GABAA antagonist PICRO did not have any effect. The ineffectiveness of PICRO on the modulation of FK effects in D. pulex found by Weiss et al.11 might indicate species differences resulting from different receptor amino acid sequences. For example, GABAA receptor subtypes with a single amino acid replacement make the Drosophila GABAA receptor PICRO-insensitive36. Indeed, in crustaceans, lobster GABAA receptors were also found to be insensitive to PICRO37. There is also the possibility that FK-mediated changes in phototactic behaviour and life history traits may be controlled by different mechanisms6.Reported information on the modulatory effects of cholinergic compounds on anti-predatory defences in Daphnia is limited to invertebrate predatory cues, which, according to previous studies, should be regulated by neurological mechanisms distinct from those of fish2,11. Our results showed that the neurological cholinergic mechanisms that modulate induced defence responses against invertebrate predators or that mimic these responses are also able to do the same for fish predation but in the opposite way. Physostigmine and carbaryl, which are acetylcholinesterase inhibitors that increase acetylcholine receptor activity, enhanced and mimicked, respectively, the morphogenetic effects of invertebrate kairomones in several Daphnia species11,21,23. Conversely, atropine, which is a muscarinic acetylcholine receptor (AChR) inhibitor like SCOP, diminished neck tooth formation in D. pulex11,21. In our study, SCOP alone abolished the positive phototactism of the studied clone, which mimicked the effects of the FKs. Conversely, PILO, which is a muscarine AChR agonist, ameliorates the phototactic responses to FKs.The nicotinic AChR agonists (NICO, IMI) and antagonist (MEC) only marginally affected the phototactic responses to the FKs. This indicates that muscarinic cholinergic signalling but not nicotinic signalling is involved in phototaxis/phototactic behaviour. It is therefore possible that both FK and SCOP treatment, through inhibition of muscarinic cholinesterase receptor activity, diminished the positive phototaxis of the studied clone, and PILO activation of these receptors ameliorated the effects of the FKs. In insects, neurons that connect olfactory inputs to higher-order brain areas that coordinate behavioural responses are thought to be under cholinergic control38.In general, GABA is known to have inhibitory functions. It has been proposed that the continuous activation of the GABAergic neuronal pathway by endogenous GABA without predatory cues prevents life history shifts11, which in our case would be the transition from positive to negative phototaxis. FKs and PICRO relieve inhibition, which can be re-established by the experimental application of GABAA receptor agonists such as DZP or GABA itself. Our results and those of Weiss et al.11 agree with the previous argument.Equi-effective mixtures of the tested agonists and antagonists had similar effects on D. magna responses to FKs as the single mixture compound treatments did, indicating that the joint effects of agonists and antagonists of the GABAergic and cholinergic signalling pathways can act cooperatively and probably independently, modulating the effects of FKs. This is in line with other findings that showed that key ecophysiological responses in Daphnia are regulated by several signalling receptor pathways, which likely ensures more robust control. This is the case for the storage lipid dynamics associated with moulting and reproduction39.The involvement of additional neurotransmitter signalling pathways, such as the serotonergic pathway, can also be taken into consideration despite being less consistent. Agonists of the serotonin receptor (such as serotonin) or treatments that increase serotonin levels (such as fluoxetine) ameliorated the effects of the FKs in only one experiment, but treatments that decreased serotonin, such as PCPA, increased the effects of the FKs in two out of the three experiments. Previously, we reported that serotonin activity in the brains of D. magna increased with algae food levels, and thus, the effects of fluoxetine on the enhancement of brain serotonin levels could only be observed under limited food conditions24. This indicates that the high levels of food used in our experiments probably prevented fluoxetine from increasing the already high serotonin levels in the central nervous system. Interestingly, inducible fish kairomone changes in phototactic behaviour in Daphnia increased with food level40, which is probably related to high levels of serotonin. On the other hand, the effects of PCPA, which decreases serotonin concentrations26, are unlikely to be modulated by food since this drug inhibits tryptophan hydrolase, the serotonin synthesis rate-limiting enzyme in D. magna41. This is apparently the case in our study.Neurophysiological stimulation experiments with dopaminergic/adrenergic agonists and antagonists were inconclusive since in only one out of two experiments the dopaminergic agonist APO diminish negative phototaxis after FK exposure. We also did not find any effects from the glutamatergic agonists and antagonists on phototactism. This could be related to the low stability of dopaminergic compounds in water and the reported small effects of glutaminergic compounds on the Daphnia motile response to light34.Consistent failure of the tested antihistaminergic drugs to modulate phototactism to visible light disagrees with previous findings that discovered that these drugs affected phototactism but at much higher doses12.Metabolomic changesThe study of metabolomic changes across the treatments that modulated FK-mediated phototactic changes or altered phototaxis provided further experimental evidence of the involvement of key neurological signalling metabolic pathways. Caution must be exercised, however, since the studied receptor agonist and antagonist drugs do not change the neurotransmitters or their related metabolites. Nevertheless, little is known about how these drugs may affect the Daphnia neuronal metabolome. The cholinergic neurotransmitter system is one of the most important systems that plays a pivotal role in learning and memory in animal species, including D. magna34,42. Whole-body concentrations of acetylcholine decreased in females exposed to FKs and those exposed to SCOP and increased in those exposed to the agonists PILO and DZP. Thus, it is possible to establish a direct link between the decreased levels of acetylcholine and decreased positive phototactism in the studied clone. The results obtained for the GABAergic and serotonergic signalling pathways were less convincing, as FKs alone did not consistently affect the levels of GABA and serotonin. However, co-exposure to FK and the GABAA receptor agonist DZP increased endogenous GABA levels, which is in line with the results reported by Weiss et al.11, who also found that the addition of exogenous GABA ameliorated FK effects. Interestingly, the summarized results depicted in Fig. 4 showed that serotonin levels dereased upon exposure to SCOP, PICRO and PILO but PILO also increase the levels of the serotonin degradation metabolite 5-HIAA. This may indicate that PILO may affect the turnover rather than the levls of serotionin.Previous findings have reported altered responses to light in D. magna individuals lacking serotonin16. Therefore, it is possible to establish a link between the observed marked negative phototactism of females exposed to SCOP and low levels of serotonin.Dopaminergic- and adrenergic-related metabolites deserve special attention, although there is only evidence that dopamine is involved in the proliferation and structural formation of morphological defences in Daphnia for invertebrate kairomones22. In some invertebrates, adrenergic signalling is considered to be absent, and the analogous functions are performed by octopamine43. In our study, fish kairomones and SCOP decreased the levels of dopamine and octopamine, whereas females co-treated with the agonists DZP and PILO and FKs showed relatively high levels of dopamine. In the insect Drosophila melanogaster, which shares many gene signalling pathways with Daphnia44, individuals deficient in dopamine show reduced positive phototactism45. Unfortunately, it is not possible to know whether the observed changes in DA in the whole bodies of D. magna indicate that DA is less used or used in excess. Figure 4 indicates that FK and SCOP reduced both DA and its intermediary metabolite L-DOPA. SCOP also increased the DA degradation metabolite 3-MT and two norepinephrine metabolites/neurotransmitters (NOEM, EPPY) that ultimately depend on DA. This means that FK decreased DA probably decreasing its intermediary metabolite L-DOPA, whereas SCOP decreased DA to a greater extent decreasing its intermediary L-DOPA but also increasing its turnover rate. Our neurophysiological stimulation experiments with dopaminergic active compounds are also not conclusive. This suggests that further research is needed to study the involvement of dopaminergic signalling in the response to fish. Existing studies on adrenergic signalling in daphnids indicated that β-blockers such as propranolol diminish the heart rate46 and motile responses to light27, which are related to the known role of adrenergic signalling that regulates blood pressure47 and other fight-or-flight responses to stress48. Future research is needed to elucidate the involvement of OCT, EPPY and NORM in the phototactic response of D. magna to FKs.In summary, this study provides consistent results that muscarinic cholinergic and GABAergic receptor agonists and antagonists are able to ameliorate or enhance, respectively, the phototactic response of adult females from the studied D. magna clone to FKs. Furthermore, inhibition of the muscarinic acetylcholine receptor by SCOP induced the phototactic response to fish kairomones. This may indicate that muscarinic cholinergic antagonists changed phototaxis, whereas muscarinic cholinergic agonists and GABAergic agonists and antagonists changed the perception of FKs. Serotonergic agonists and antagonists were also able to diminish and increase FK effects, respectively, but only in half of the trials performed. The fact that we could not observe effects from the remaining neuroactive agents (i.e., dopaminergic, histaminergic, glutamatergic) could simply be because they are not relevant for predator-induced anti-phototaxis. The study of neurotransmitters and their related metabolite changes allowed us to identify acetylcholine and GABA as putative key metabolites associated with the observed phototactic modulatory effects of FK and cholinergic and GABAergic compounds. Increased and decreased levels of dopamine in the whole bodies of D. magna were related to positive and negative phototactic behaviours, respectively, but could not be related to neurophysiological studies with the tested dopaminergic drugs. More

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    Illegal mining in the Amazon hits record high amid Indigenous protests

    Indigenous territories, long a bulwark against deforestation in the Amazon, are under increasing threat in Brazil, according to an analysis of 36 years’ worth of satellite imagery. The data show that illicit mining operations on Indigenous lands and in other areas formally protected by law have hit a record high in the past few years, under the administration of President Jair Bolsonaro, underscoring fears that his policies and rhetoric are undermining both human rights and environmental protection across the world’s largest rainforest. These operations strip the land of vegetation and pollute waterways with mercury.
    When will the Amazon hit a tipping point?
    The analysis, released in late August, comes as scientists and environmentalists warn of a deteriorating situation in Brazil; Indigenous groups have frequently found themselves in violent clashes with miners since Bolsonaro took office in 2019 — and they are demanding more protection for their land. Although Indigenous territories are legally protected, Bolsonaro has openly called for mining and other development in them.“This is definitely the worst it’s been for Indigenous peoples since the constitution was signed in 1988,” says Glenn Shepard, an anthropologist with the Emílio Goeldi Museum in Belém. Before this, Brazil was ruled by a military dictatorship.Researchers at MapBiomas, a consortium of academic, business and non-governmental organizations that has been conducting geospatial studies across Brazil, developed algorithms that they used in conjunction with Google Earth Engine to conduct the analysis. After training the algorithms on images of mining operations — desolate landscapes where forests have been converted into a collection of sand dunes pockmarked by mining ponds — the team ran its analysis on a freely available archive of imagery captured by the US Landsat programme, and then analysed trends on Indigenous lands and other formally protected areas where mining is not allowed.Over the past decade, illegal mining incursions — mostly small-scale gold extraction operations — have increased fivefold on Indigenous lands and threefold in other protected areas of Brazil such as parks, the data show (see ‘Mining incursions’). The findings agree broadly with reports from Brazil’s National Institute for Space Research (INPE) in São José dos Campos, which monitors the country’s forests and has been issuing alerts about mining incursions for several years. “We kind of knew that this was happening, but to see numbers like this is scary even for us,” says Cesar Diniz, a geologist with the geospatial-analysis company Solved in Belém, Brazil, who led the analysis for MapBiomas.Clashes on multiple frontsAside from being home to their people, Indigenous territories play a part in protecting the Amazon’s biodiversity and the enormous pool of carbon that is locked away in its trees and soils. Numerous studies have found that Indigenous lands, as well as other conservation areas, are effective buffers against tropical deforestation in the Amazon1,2, which is responsible for around 8% of global carbon emissions.Earlier this month, the International Union for Conservation of Nature (IUCN) approved a motion, put forward by Indigenous groups, calling on governments to protect 80% of the Amazon basin by 2025. Indigenous representatives say they plan to fight for implementation across the Amazon, but the proposal faces a particularly tough sell in Brazil under Bolsonaro, whose pro-business conservative government has scaled back enforcement of existing environmental laws and halted efforts to demarcate new Indigenous territories.

    Sources: MapBiomas/Amazon Geo-Referenced Socio-Environmental Information Network/Terrabrasilis

    Indigenous groups have also taken their case to the International Criminal Court in The Hague, the Netherlands. On 9 August, the Articulation of Indigenous Peoples of Brazil (APIB), which represents Indigenous groups across the country, filed a complaint with the court accusing the Bolsonaro administration of violating human rights and, they claim, paving a path for genocide by undermining Indigenous rights, reducing environmental protections and inciting incursions and violence through calls for mining and land development. APIB also made it clear that it’s not just Indigenous rights at stake, drawing a direct link between the protection of their territories and of the globe.

    Members of the Munduruku people sit in front of equipment from an illegal mining operation on their land.Credit: Meridith Kohut/The New York Times/eyevine

    “Defending the traditional territories of Amazonian communities is the best way to save the forest,” says Luiz Eloy Terena, an anthropologist and lawyer from the village of Ipegue who coordinates legal affairs for APIB. “What is needed is a state commitment on the demarcation and protection of Indigenous lands, which are the last barrier against deforestation and forest degradation.”During an address to the United Nations General Assembly on 21 September, Bolsonaro said he was committed to protecting the Amazon and emphasized that 600,000 Indigenous people live “in freedom” on reserves totalling 1.1 million square kilometres of land, equivalent to 14% of Brazil’s territory. In the past, Bolsonaro has publicly said that Indigenous peoples have too much land given their sparse population, and at times called for their “integration”. The Bolsonaro administration did not respond to Nature’s requests for comment regarding illegal mining in the Amazon, its Indigenous and environmental policies or the accusations filed with the International Criminal Court.Existential threatBrazil earned recognition as a leader in sustainable development during the 2000s. Former president Luiz Inácio ‘Lula’ da Silva and his Workers’ Party put in place policies that helped to curb deforestation in the Amazon by more than 80% between 2004 and 2012.

    Source: Brazilian National Institute for Space Research

    But the party was dogged by corruption charges that would later land Lula in jail, and its environmental agenda ultimately faltered. In 2012, the increasingly conservative Brazilian Congress weakened a once-vaunted forest-protection law. With each successive government, funding for the country’s main environmental enforcement agency, the Institute of Environment and Renewable Natural Resources (IBAMA), has decreased: IBAMA had 1,500 enforcement agents in 2012, compared with just 600 today, says Suely Araújo, a political scientist in Brasília who spent nearly three decades working in the Brazilian Congress and led IBAMA from 2016 to 2018.The rate of deforestation in the Amazon, which includes land converted for mining, agriculture and other development, began rising anew after 2012 and shot up by 44% during Bolsonaro’s first two years in office, according to INPE (see ‘Razing the rainforest’). Many expect yet another increase when the numbers for 2021 are released later this year.But the biggest threats are yet to come, says Araújo. The current government is now pushing legislation in Congress — as well as arguments in a case that is pending before Brazil’s Supreme Court — that would make it harder to establish new Indigenous lands and could even allow the government to repossess existing lands. Other legislation that has been advanced by Bolsonaro’s supporters in Congress would open up Indigenous lands to industrial development, grant amnesty to people who have illegally invaded public lands and gut regulations governing major infrastructure projects such as mines, roads and dams.
    The scientists restoring a gold-mining disaster zone in the Peruvian Amazon
    “It’s painful,” says Araújo, who decided to forgo retirement and join Brazil’s Climate Observatory, a coalition of activist and academic groups fighting to preserve the country’s social and environmental protections. “This has become my mission.”For Indigenous tribes, the growing damage to their lands and the rainforest pose an existential threat. More than 6,000 Indigenous people descended on Brasília, the country’s capital, in August and September in protest against Bolsonaro’s policies on land demarcation and the environment. They also travelled to Marseille, France, for the IUCN’s World Conservation Congress earlier this month to promote their motion to protect the Amazon basin.“We will not give up,” says José Gregorio Diaz Mirabal, a member of the Wakueni Kurripaco people of Venezuela and the elected leader of the Congress of Indigenous Organizations of the Amazon Basin. “Science supports us, and the world is waking up.”

    doi: https://doi.org/10.1038/d41586-021-02644-x

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