So long suckers: Estimating species diversity in a unique but imperiled Amazon catfish fauna

Brazil, as many other South American nations, has experienced a period of rapid economic growth accompanied by expanding energy needs. To meet its energetic needs, Brazil has invested heavily in hydroelectic power generation such that ~80% of Brazil's electricity production is met by hydropower. 55% the hydroelectric potential still awaits exploitations and the Amazon basin is the next and last hydroelectric frontier, with plans for the construction of 200+ dams, leaving only 3 unimpounded Amazon tributaries.

Hydroelectric projects are build on high energy, steep gradient sections of rivers that are characterized by rapids and waterfalls. These river sections provide habitat for unique and distinct rheophilic fauna and flora which inevitably are destroyed as a result of hydropower development. The rheophilic fauna is relatively poorly known, leading to a severe underestimation of the real impact of hydropower development in the Amazon basin.

ResultsA total of 870 ancistrin loricariid specimens were collected from

the Xingu and Tapajós, comprising 190 lots. From these lots, we generated DNA barcodes for 447 individuals, comprising 169 unique haplotypes. Median barcode sequence length was 624 bp (max=630, min=336), with five below 500 bp.

Using molecular methods, species richness point estimates varied between 32 and 44 species according to method. GMYC estimated 44 species (mode=42; 95% CI=35–52); bGMYC estimated 39 species (mode=39; 95% CI=21–42); locMin (threshold optimized at 0.016) estimated 37 species (mode=37; 95% CI=25–55); mPTP estimated 32 species (mode=33; 95% CI=25–37). From the Xingu, between 18 and 24 species were estimated with the molecular methods, and from the Tapajós between 22 and 23.

From morphological assessments we assigned the voucher specimens to 16 genera, 27 nominal species (specific epithets), 59 morphotypes under the liberal criterion, 45 morphotypes under the strict criterion, and 43 morphotypes that corresponded to L-numbers. Of these, from the Xingu we report 38 morphotypes (strict), 29 morphotypes (liberal), 25 L-numbers, and 18 nominal species; from the Tapajós we report 23 morphotypes (strict), 22 morphotypes (liberal), 19 L-numbers, and 15 nominal species.

DiscussionWhen looking at wider patterns across the drainages, it is clear

that within-drainage endemism is high. Despite the Xingu and Tapajós rivers apparently having a shared faunal history, only two species—Peckoltia sabaji and Panaque armbrusteri, possibly Scobinancistrus pariolispos—were found in our analyses as the same species inhabiting both drainages. Members of almost all genera were found in both rivers, with absences, e.g. Acanthicus, being explained by insufficient sampling rather than real absence. Two supposedly shared species, Peckoltia vittata and Baryancistrus niveatus, were recovered by all methods as distinct species in each river. We also report intra-drainage divergences, with eleven of the sixteen genera (nearly 70%) having multiple sympatric species within drainage. Interestingly, some of the sampled tributaries appear to harbour endemics, and these rivers have dramatically different geology and water chemistry to the main river.

ConservationSpecies richness was found to be substantially higher than

would be inferred from species lists of taxonomic names alone, and together with high levels of between- and within-basin diversity and possible endemics in tributaries, it is demonstrated the rapids habitats of the Xingu and Tapajós are of immense biological diversity and conservation value. Therefore, similarly to other tropical rapids systems such as the lower Congo, the extensive rapids of the Xingu and Tapajós are likely to be areas of active speciation for rheophilic organisms due to their complex hydrology. Only by combining approaches we were able to reveal this diversity, as our molecular methods alone underestimated species richness, an unfortunate observation highlighted by Isambert (2011): “ranking sites for conservation priority based solely on PD [phylogenetic diversity, i.e. branch lengths] potentially disfavor endemic species by under-rating areas where the evolutionary process is most active”. Therefore future studies need to be aware of methodological biases in order not to overlook the kinds of biological systems that need the most protection.

Isambert et al. (2011) Endemism and evolutionary history in conflict over Madagascar's freshwater conservation priorities. Biological Conservation, 144, 1902-1909. doi:10.1016/j.biocon.2011.04.016GMYC: Fujisawa & Barraclough (2013) doi:10.1093/sysbio/syt033bGMYC: Reid & Carstens (2012) doi:10.1186/1471-2148-12-196locMin: Brown et al. (2012) doi:10.1111/j.1755-0998.2011.03108.xmPTP: Kapli et al. (2017) doi:10.1093/bioinformatics/btx025

This research was supported by the MCT/CNPq/PPG7 557090/2005-9, CNPq/CT-Amazonia 554057/2006-9, CNPq/CT-Amazonia 575603/2008-9 and CNPq/FAPEAM/SISBIOTA (Rede BioPHAM) 563348/2010 to I.P.F. and CNPq 483155/2010-1, CNPq 490682/2010 and CNPq 400813/2012-2 to T.H.

The environmental impact of large infrastructure projects hinges upon estimates of species richness and endemism, yet much tropical biodiversity is poorly known. Two major tributaries of the Amazon in Brazil—the Xingu and Tapajós rivers—are under immediate threat from extensive hydroelectric dam development schemes, the ultimate impacts of which are unknown but are likely to be serious. Using molecular techniques (COI barcodes), we perform a species inventory of suckermouth catfishes (Siluriformes: Loricariidae: Ancistrini), a key functional group and a diverse component of lotic ecosystems in the Neotropics. With multiple species discovery methods (GMYC, bGMYC, locMin OTU clustering, mPTP), and by accommodating phylogenetic uncertainty, we address potential sources of bias, and compare these results to an assessment of diversity using morphotyping. Confidence intervals around species richness were wide, reflecting the impact of phylogenetic uncertainty and methodological bias, but results remained consistently lower (33–42 species) than for the estimated number of morphotypes (45–59). These discrepancies highlight a situation critical for determining conservation priorities from baseline inventories of biodiversity, whereby single locus methods can fail to identify groups undergoing recent/ongoing speciation or introgression, only being identified with the inclusion of a morphological overview. Conversely, molecular methods provide crucial information on relationships and timings of diversification, and can additionally reveal instances where subtle morphologies are obscuring speciation events. We also report substantial within-drainage endemicity, with ~70% of genera having multiple conspecifics, many of which are likely to have diversified in situ. We conclude that any hydroelectric dam projects of the scale proposed are likely to have a profound effect upon the significant diversity these globally important geological and hydrological systems are capable of producing.

Tomas Hrbek1, Rupert A. Collins1,2, Emanuell Ribeiro1,3, Izeni P. Farias1

1Laboratório de Evolução e Genética Animal, Departamento de Genética, Universidade Federal do Amazonas (UFAM), Manaus, AM, Brazil2School of Biological Sciences, Life Sciences Building, University of Bristol, UK

3Departmento de Biologia, Universidad de Puerto Rico, San Juan, PR4Programa de Pós-Graduação em Ecologia Aquática e Pesca, Instituto de Ciências Biológicas, Universidade Federal do Pará (UFPA), Belém, Pará, Brazil

Ancistomus snethlageae 'L141'

Hypancistrus sp. 'L262'

Ancistomus snethlageae 'L141'

Baryancistrus niveatus 'L142'

Pseudacanthicus sp. 'L273'

Leporacanthicus joselimai 'L264'

Baryancistrus niveatus 'L142'

Baryancistrus niveatus 'L142'Baryancistrus niveatus 'L142'

Baryancistrus niveatus 'L142'

Hypancistrus sp. 'L262'

Pseudacanthicus sp. 'L273'

Hopliancistrus tricornis 'L212'

Ancistrus sp. 'L309'

Ancistrus sp. 'Pimental'

Pseudancistrus zawadzkii 'L321'

Pseudancistrus zawadzkii 'L259'

Ancistomus snethlageae 'L141'Ancistomus snethlageae 'L141'

Baryancistrus niveatus 'L142'Baryancistrus niveatus 'L142'

Pseudancistrus zawadzkii 'L259'

Pseudancistrus zawadzkii 'L321'

Ancistomus snethlageae 'L141'Ancistomus snethlageae 'L141'

Ancistomus snethlageae 'L141'

Hopliancistrus tricornis 'L212'

Ancistrus sp. 'L309'Ancistrus sp. 'L309'

Scobinancistrus pariolispos 'L368'

Ancistrus sp. 'L309'

Baryancistrus niveatus 'L142'

Hypancistrus sp. 'L260'

Peckoltia vittata 'L140'

Peckoltia sabaji

Pseudacanthicus sp. 'L273'

Ancistomus snethlageae 'L141'

Ancistrus sp. 'L213'

Ancistrus sp. 'Pimental'

Ancistrus sp. 'Pimental'Ancistrus sp. 'Pimental'

Peckoltia sabaji

Peckoltia vittata 'L140'

Peckoltia vittata 'L140'

Spectracanthicus immaculatus 'L269'Spectracanthicus immaculatus 'L269'

Hypancistrus sp. 'L260'

Ancistomus snethlageae 'L141'

Hypancistrus sp. 'L260'Hypancistrus sp. 'L260'

Peckoltia cavatica 'L265'Peckoltia cavatica 'L265'Peckoltia cavatica 'L265'

Spectracanthicus murinus

Ancistrus sp. 'L213'

Spectracanthicus immaculatus 'L269'

Lasiancistrus schomburgkii

Ancistrus dolichopterus 'L071'

Spectracanthicus murinus

Ancistrus sp. 'L213'

Pseudancistrus zawadzkii 'L321'Pseudancistrus zawadzkii 'L321'

Scobinancistrus pariolispos 'L368'

Leporacanthicus joselimai 'L264'

Panaque armbrusteri 'L027'

Peckoltia compta 'L134'

Hypancistrus sp. 'L262'

Pseudacanthicus sp. 'L097'

Baryancistrus xanthellus 'L018'

Baryancistrus xanthellus 'L018'

Parancistrus sp. 'L332'

Hopliancistrus sp. 'L017'

Hopliancistrus sp. 'L017'

Spectracanthicus punctatissimus 'bicudo L315'

Spectracanthicus zuanoni 'smallmouth dark'

Ancistrus sp. 'L100'

Ancistrus sp. 'pintinha'

Ancistrus sp. 'pintinha'Ancistrus sp. 'pintinha'

Ancistrus sp. 'pintinha'

Ancistrus sp. 'pintinha'

Pseudancistrus asurini 'L067'

Baryancistrus niveatus 'L019'Baryancistrus niveatus 'L019'

Peckoltia vittata 'L015'Peckoltia vittata 'L015'

Spectracanthicus zuanoni 'widemouth bigspot L354'Spectracanthicus zuanoni 'widemouth bigspot L354'

Ancistomus feldbergae 'L013'

Spectracanthicus punctatissimus 'bicudo L315'

Spectracanthicus punctatissimus 'bicudo L315'

Spectracanthicus zuanoni 'smallmouth dark'

Spectracanthicus zuanoni 'smallmouth dark'

Baryancistrus xanthellus 'L018'

Baryancistrus xanthellus 'L018'

Baryancistrus xanthellus 'L018'

Baryancistrus xanthellus 'L018'

Baryancistrus xanthellus 'L018'

Spectracanthicus punctatissimus 'bicudo L315'

Scobinancistrus aureatus 'L014'

Baryancistrus xanthellus 'L018'

Spectracanthicus zuanoni 'smallmouth dark'Spectracanthicus zuanoni 'smallmouth dark'

Spectracanthicus zuanoni 'smallmouth dark'

Baryancistrus xanthellus 'L018'Baryancistrus xanthellus 'L018'

Baryancistrus xanthellus 'L018'

Spectracanthicus punctatissimus 'bigspot'

Spectracanthicus zuanoni 'smallmouth dark'

Spectracanthicus zuanoni 'bigeye widemouth'Spectracanthicus zuanoni 'bigeye widemouth'

Ancistomus feldbergae 'L013'

Ancistrus ranunculus 'L034'

Spectracanthicus zuanoni 'smalleye smallmouth'Spectracanthicus zuanoni 'smalleye smallmouth'

Hopliancistrus sp. 'L017'

Parancistrus nudiventris 'L031'

Pseudancistrus asurini 'L067'

Hypancistrus sp. 'L174'

Scobinancistrus pariolispos 'L048'Scobinancistrus pariolispos 'L048'

Peckoltia sabajiPeckoltia sabaji

Ancistrus ranunculus 'L034'Ancistrus ranunculus 'L034'

Ancistrus sp. 'L100'

Spectracanthicus zuanoni 'smalleye smallmouth'

Spectracanthicus zuanoni 'bigeye widemouth smallspot'

Baryancistrus xanthellus 'L177'

Leporacanthicus heterodonLeporacanthicus heterodon

Spectracanthicus punctatissimus 'shortsnout smallspot'

Spectracanthicus punctatissimus 'bicudo L315'

Spectracanthicus punctatissimus 'bicudo L315'

Spectracanthicus punctatissimus 'shortsnout smallspot'

Ancistomus snethlageae 'L161'

Hopliancistrus sp. 'L171'Hopliancistrus sp. 'L171'

Baryancistrus xanthellus 'L177'

Spectracanthicus punctatissimus 'bigeye widemouth'

Peckoltia vittata 'L015'

Ancistrus sp. 'pintinha'

Baryancistrus xanthellus 'L018'

Hypancistrus sp. 'L066'Hypancistrus sp. 'L066'

Hypancistrus sp. 'L066'

Panaqolus tankei 'L398'

Panaque armbrusteri 'L027'

Spectracanthicus zuanoni 'smalleye smallmouth'Spectracanthicus zuanoni 'smalleye smallmouth'

Spectracanthicus punctatissimus 'bigeye widemouth'

Ancistrus ranunculus 'L034'Ancistrus ranunculus 'L034'

Peckoltia vittata 'L015'

Pseudancistrus asurini 'L067'

Baryancistrus sp. 'verde'

Hopliancistrus sp. 'pinta'

Pseudancistrus asurini 'L067'

Scobinancistrus sp. 'L082'

Pseudacanthicus sp. 'L185'

Acanthicus hystrix 'L155'

Peckoltia vittata 'L015'

Spectracanthicus punctatissimus 'shortsnout smallspot'

Spectracanthicus punctatissimus 'bicudo L315'

Baryancistrus sp. 'verde'

Baryancistrus sp. 'verde'

Baryancistrus sp. 'verde'

Hypancistrus sp. 'L066'Hypancistrus zebra 'L046'

mPTP

locM

in

bGMYC

GMYC

0.00

0.05

0.10

0.15

20 30 40 50 60

Estimated number of species

Dis

trib

utio

n ke

rnel

den

sity

bGMYC

GMYC

locMin

mPTP

Nominal L-Numbers Strict Liberal

L-177

L-46

Pekoltia sabaji

L-264

L-14

L-15

ID: 615