Fishes from Yarinacocha lake: an emblematic Amazonian ecosystem in the lower Ucayali River basin, Pucallpa, Peru

Abstract The Yarinacocha lake is an emblematic ecosystem of the Peruvian Amazon, representing the main point of fish landing and a tourist attraction in the city of Pucallpa. The wide fauna diversity in this area has made it the target of various studies, although for fish species most of them were focused on commercial species. In this work, we carried out the first ichthyofauna species inventory of the Yarinacocha lake, sampling throughout the entire lake during the rainy and dry seasons and considering also all previously recorded species deposited in the Ichthyological Collection of the MUSM with the same locality. A total of 164 fish species were recorded, representing 10 orders (plus Eupercaria), 34 families and 116 genera. Characiformes was the order with more species (68 spp., 41.5%) followed by Siluriformes (59 spp., 36%), Cichliformes (17 spp., 10.5%), and Gymnotiformes (8 spp., 4.9%). The most highly represented families, including almost 55.5% of the total diversity obtained, were Characidae (23 spp., 14%), followed by Cichlidae (17 spp., 10.4%), Loricariidae (14 spp., 8.5%), Pimelodidae (13 spp., 7.9%), Doradidae (13 spp., 7.4%) and Anostomidae (12 spp., 7.3%). From the total fish species recorded in this study, only 22 are considered protected species following the IUCN criteria and 109 species have commercial importance, including 90 ornamental species (54.8%). Our results contribute to the knowledge of the ichthyofauna of the Yarinacocha lake and can be used as a starting point for its conservation and sustainable management over time.


Introduction
The Peruvian Amazonian ichthyofauna has been the object of numerous and in-depth studies, which register more than 800 species (Ortega et al. 2012).Among lotic water bodies, the most important assessments include the Amazon (Goulding et al. 2003), Huallaga (Ortega et al. 2007), Madre de Dios (Barthem et al. 2003), Aguaytía (Quezada et al. 2017) and Las Piedras (Carvalho et al. 2011) River basins.Likewise, the lentic aquatic ecosystems of the Peruvian Amazon play an important ecological role and contribute to the support of economic activities of the local population (García-Vásquez et al. 2009) due to its value as a source of hydrobiological resources.This is partially the consequence of oxbows migration, which promotes this enormous diversity forming sinuous rivers and lakes during the course changes (Nagel et al. 2022), and the flood pulses that comprise annual oscillations of the average water level (Junk et al. 1989), allowing the interconnection of lakes and small water bodies during the floods (Bartletta et al. 2010).
The Yarinacocha lake, located in the district of Yarinacocha, department of Ucayali, known regionally as "cocha" or "tipishca" by shipibo-conibo populations, is approximately 20 km long, with an area of 13.4 km 2 , a maximum depth of 19 m and average width of 650 m (Campbell et al. 2017).Its meandering origin formed by the erosion of Ucayali River banks (Neuendorf et al. 2005) has allowed the occurrence of an enormous diversity, not yet fully monitored, but which supports important fishing activities in the region, local consumption and tourist destination (García-Dávila et al. 2018).During the floods of the Ucayali River in January, February and March, the entire lake acts as a riverside highway for trade and transportation (Campbell et al. 2017).The rest of the year it is supplied with water from small tributaries that can be streams or "caños", which are small channels that connect the lake with other water bodies and represents a key habitat for many species of fish reproduction (MINAM 2021).However, as a result of the human populations growth on the riverbanks (hamlets, communities and the population of the Yarinacocha district), restaurants and tourism, the use of toxic substances in illegal fishing and by hospital wastewater that fail biodiversity and human health (personal comments by José Riofrío), this ecosystem is highly polluted by sewage and solid waste that could affect biodiversity (Rondon-Espinoza et al. 2022).These characteristics and threats as a whole, give Yarinacocha lake an emblematic meaning covering cultural, economic and ecological aspects worthy of being preserved and studied.
Scientific knowledge of the fish species composition at Yarinacocha lake is limited.A recent study reports that the diversity of fish species that arrives at the Yarinacocha lake landing stage, including a large part of the Utuquinía and Callería sub-basins, and to a lesser extent Loreto and Aguaytía-San Alejandro (Salazar- Ramirez et al. 2021).In their results, 63 species between 2015 and 2019 were reported, being the most abundant "carachama" (Loricariidae), "piro" (Doradidae), "palometa" (Mylossoma spp.) and "sardina" (Triportheus spp.) all of them recorded only as common names that may include several species.Other studies include monitoring of fishing landings in the city of Pucallpa (Vela et al. 2016) and characterization of commercial fisheries in the Ucayali River basin (Zorrilla et al. 2016), without offering precise data on the ichthyofauna of the lake.Also, these studies focus on large fishes with commercial interest, while neglecting the smaller species that contain the highest biomass (Barletta et al. 2010) and to date, no other publication has reported the total diversity of the ichthyofauna of the Yarinacocha lake.
This lack of monitoring and rapid identification tools for the fish fauna of Yarinacocha lake encourages the existence of erroneous records in fishing statistics (García-Dávila et al. 2018) and could be covering up the depredation of the fish populations.
For the above stated, we have formulated as the main purpose of this work to present the first fish species checklist of Yarinacocha Lake, updating the information of continental catalogs (Reis et al. 2003), species threatened status (IUCN 2022) and economic importance of species reported.

Material and Methods
A total of 15 sampling sites were evaluated (Fig. 1, Table 1), covering variable environments inside Yarinacocha lake including streams, water channels and shores (Fig. 2).
Figure 1.Map of Yarinacocha lake, Ucayali, Peru showing each collecting site (red circles).Numbers follow Table 1 and Fig. 2. Sampling efforts occurred during the start of the rainy season in October 2020 and in the dry season in July 2022, mostly during daylight.The collection of specimens involved bottom trawls of 10 and 20 m nets with 5 mm internodes, used on the beaches and areas with vegetation, trunks and leaves; cast nets of 15 m in open areas and channels; and gillnets of 30 m, blocking the passage of fish during the beginning of the day.Obtained specimens were anesthetized in a clove oil solution, muscle tissues were fixed in 96% ethanol (for molecular studies), vouchers and other specimens were fixed in 10% formalin by 48 hours and then preserved in 70% ethanol.Expeditions had a Fish Collection Permit for research purposes under PRODUCE license number 132/2021.
Specimens collected in the Yarinacocha lake by previous expeditions and deposited in the MUSM Fish Collection, were also recorded after their identifications were verified.In our results, only native species were included without considering invasive or exotic species because they lacked vouchers in the scientific collection; however, its presence was discussed due to previous reports from the Ministerio del Ambiente (MINAM).

Results and Discussion
The total of previously reported species is 63 (Vela et al. 2016;Zorrilla et al. 2016;Salazar-Ramirez et al. 2021) reporting only Characiformes and Siluriformes.However, as indicated above, those studies did not include precise data on the location of capture, making impossible a comparison of the total richness previously reported in relation to the results presented here which only include fishes from Yarinacocha lake.
Our contribution carries a very high value due to the fact of representing the first ichthyofauna inventory of Yarinacocha lake in its entire extension, assessing a wide range of habitats, including almost all possible species, not only those with commercial value (Fig. 3).In this manner, a total 164 fish species were recorded (Table 2) representing 10 orders (plus Eupercaria), 34 families and 116 genera.
The following species could not be identified to the species level Hemiodus aff.microlepis belongs to the Hemiodus microlepis species group, previously reported for the Ucayali River, being a species not formally described (Nogueira et al. 2021), Leporinus cf.parae, a member of the Leporinus friderici species complex (Silva-Santos et al. 2018), and Leporinus aff.amazonicus represents putative undescribed species.Leporinus is the most species-rich genus within Anostomidae and is considered one of the richest genera within Characiformes (Garavello andBritski 2003, Ramirez et al. 2016) and a thorough taxonomic review of this group is needed (Silva-Santos et al. 2018).Rineloricaria sp. could only be identified to the genus level without coinciding with R. morrowi or R. wolfei, the two species described for the region by Fowler (1940), further studies will be needed to classify these specimens.Moenkhausia aff.dichroura belongs to the M. dichroura species group, because it's distributed only in the La Plata basin (Paraguay and lower Paraná rivers) and the morphotype found in the Amazon basin would be a possible new species (Britzke 2011).Several species have the same color pattern, such as M. dichroura, M. intermedia, M. barbouri, M. bonita and also the species Schultzites axelrodi, which in some cases may make it difficult to correctly identify this species group.
Regarding the species of economic importance, 109 species have commercial importance, of which 90 species (54.8%) are ornamentals, 26 species are used for both purposes and 20 species only for consumption, including Prochilodus nigricans (boquichico) which contributes the highest percentage of catches (Riofrío 1998, Biota Neotrop., 23(1) The reduction in landings in Yarinacocha lake has been reported in recent years (Salazar-Ramirez et al. 2021).Species of consumption of high commercial demand such as Colossoma macropomum (gamitana) and Piaractus brachypomus (paco) have almost disappeared from landings, being replaced by small-sized species (Riofrío 1998, Wasiw et al. 2012, Salazar-Ramirez et al. 2021).This evidences the decrease of fish populations for consumption due to overexploitation.
The global ornamental fish industry is a market expansion grid, and moves approximately US$ 15 billion/year, including equipment, accessories, supplies and publications (Cheong 1996).There are 350 to 400 million ornamental fish sold, where 70% are produced in captivity and 63% are exported by developing countries generating about U.S. $ 202 million/year (Chao et al. 2001).This market is dominated by freshwater fishes and the Amazon basin is a key supplier of wild freshwater fishes to the ornamental trade (Moreau and Coomes 2007).In the Peruvian Amazon, most of these resources are the product of direct extraction from the natural environment (MINAM 2021) and Yarinacocha lake is one of the leading regions for ornamental fish extraction in the Ucayali department (PNIPA 2021).Although the collection of fish from tropical lentic environments can be carried out almost throughout the entire year, this activity can lead to direct depletion of wild populations (Andrews 1990).
In recent years, the global trade for freshwater specimens has led to the overexploitation of native species, and the destruction of these habitats by invasive species (Chang et al. 2009).An example of an exotic species found in Peru would be Trichopodus trichopterus (Pallas 1770), order Anabantiformes, family Osphronemidae, that was reported in Yarinacocha in 2016, in the La Restinga fishing area (MINAM 2021).This species is a tropical freshwater fish native to Southeast Asia, known as the three spot gourami, and has a specialized organ (organ labyrinth) that allows them to breathe oxygen from the air (Blank & Burggren 2014), helping them to adapt to an environment of low oxygen concentration in the water (Degani et al. 2021).Specimens of this group were introduced in 1970 for ornamentation (Ortega et al. 2007) and have been reported for the city of Iquitos (department of Loreto, Peru) (Meza-Vargas et al. 2021).The effects of exotic species on lentic water bodies can be complex (Ortega and Hidalgo 2008), although the impact of T. trichopterus on native species is uncertain, the introduction of exotic species may imply a risk of co-introduction of parasites, especially with phylogenetically similar native fauna (Trujillo-González et al. 2018), and generate problems of predation, competition for food and occupation of niches (Meza-Vargas et al. 2021).Therefore, T. trichopterus can be detrimental to native fish and further studies are required to assess the real impact on native species.
Freshwater fish may currently be one of the most threatened vertebrate groups, mainly based on the more than 5,000 species assessed by the IUCN, where the main threats include habitat modification, fragmentation and destruction; the introduction of invasive species; fisheries overexploitation; environment pollution; and climate change (Reid 2013).Thus, in the long term, it is estimated that 20% of the world's freshwater fish should be in the vulnerable, threatened or extinct category in recent decades (Revenga et al. 1998).
In this study, 22 species are considered protected species (13.4%) following the IUCN criteria.One species, Arapaima gigas, was categorized as "Data deficient" (DD), therefore the knowledge about the biology and ecology of this species is limited, in particular the structure of its natural populations (Vitorino et al. 2017) and further information on the species is required.The natural populations of this species have historically been reduced or even eradicated near the main cities (Castello et al. 2011).Currently, its landing in Yarinacocha lake is almost nil (Salazar-Ramírez et al. 2021).The other 21 species are considered "Least concern" (LC), which means that after being evaluated, it doesn't meet any of the criteria that define the other categories.Most of the registered species lack information that allows them to be classified in some category, therefore further studies are necessary for an adequate evaluation of these species and of the Peruvian ichthyofauna in general.
Overall, Yarinacocha lake is an ecosystem with a high diversity of fish species that are valuable resources for the local people.Nonetheless, these resources are vulnerable to pollution, overexploitation and the presence of exotic species that affect native populations.Our study contributes to the knowledge of the ichthyofauna of the Yarinacocha lake and can be used as a starting point for its conservation and sustainable management over time.

Figure 4 .
Figure 4. Richness of fish species for orders/series recorded in Yarinacocha lake.

Figure 5 .
Figure5.Richness of fish species for families recorded in Yarinacocha lake.

Table 1 .
Sampled localities in the Yarinacocha lake.

Table 2 .
Fish fauna recoGarcía Dávila et al. (2021)ke.The list includes the Peruvian common name, economic importance of the species as ornamental fish (O) according toIIAP (2011) andGarcía Dávila et al. (2021), or fish for consumption (C) according toGarcía-Dávila et al. (2018), IUCN category (LC = Least Concern, DD = Data Deficient, NT = Near Threatened, CR = Critically Endangered, EN = Endangered, VU = Vulnerable).In addition, the catalog number of the voucher specimens deposited in the MUSM fish collections is also being considered.