Published in November 2021
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Viewpoint
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Rocío A. Baquero, Daniel Ayllón, Francisco J. Oficialdegui and Graciela G. Nicola
Tackling biological invasions in Natura 2000 network in the light of the new EU Biodiversity Strategy for 2030 (pp 776–791) |
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The European Commission has recently adopted its EU Biodiversity Strategy for 2030, which sets out an ambitious plan for reversing
biodiversity loss, and preserving and restoring protected ecosystems. A central binding target is focused on enlarging the EU network
of legally protected areas (Natura 2000, the largest global network of the world), and on maintaining or improving the conservation
status of all vulnerable habitats and species included in them. Biological invasions are currently a major threat to Natura 2000,
so fulfilling the objectives of the EU Biodiversity Strategy calls for stepping up the implementation and enforcement of the relevant
legislation on the matter, which has been thoroughly revised over the last decade. We discuss here the regulatory aspects of legislation
on invasive alien species (IAS) that need to be optimised to address the challenge posed by biological invasions to the Natura
2000 network in the light of the new EU Biodiversity Strategy. We highlight that, while the EU has designed a solid regulatory
framework to tackle the threat of biological invasions, its successful implementation will mainly rely upon appropriate national
enforcement and allocation of economic and human resources. Despite previous warnings, the creation of dedicated EU funding mechanisms
to support a comprehensive implementation of the legislation still remains a priority. Due to the yet small number of IAS regulated
at the EU level, prevention and management of IAS will largely depend on national and local administration efforts, and on regional
coordination and cooperation across neighbouring countries. Therefore, a well-integrated system responsible for biosecurity, pests
and invasive alien organisms at the EU level would be better accomplished through a centralized, independent EU agency of new creation.
Likewise, the establishment of a similar lead agency at the MS level, with special focus on IAS management in Natura 2000, is recommended
to navigate the existing complex regulatory framework.
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Research articles
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Mark John Costello, Stefanie Dekeyzer, Bella S. Galil, Pat Hutchings, Stelios Katsanevakis, Shyama Pagad, Tamara B. Robinson, Xavier Turon, Leen Vandepitte, Bart Vanhoorne, Kevin Verfaille, Richard C. Willan and Marc Rius
Introducing the World Register of Introduced Marine Species (WRiMS) (pp 792–811) |
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A major historical challenge for the management of anthropogenic introductions of species has been the absence of a globally standardised system for species nomenclature.
For over a decade, the World Register of Marine Species (WoRMS) has provided a taxonomically authoritative classification and designation of the currently accepted names
for all known marine species. However, WoRMS mainly focuses on taxonomy and does not specifically address species introductions. Here, we introduce the World Register
of Introduced Marine Species (WRiMS), a database directly linked to WoRMS that includes all introduced marine species, distinguishing native and introduced geographic ranges.
Both the WoRMS and WRiMS contents are continually updated by specialists who add citations of original species descriptions, key taxonomic literature, images and notes on native
and introduced geographic distributions. WRiMS editors take responsibility for assessing the validity of species records by critically evaluating if a species has been introduced
to a region, erroneously identified and/or potentially naturally present in a region but previously unnoticed. WRiMS currently contains 2,714 introduced species. The amount and
quality of the information entered depend on the availability of experts to update its contents. Because WRiMS is global and it combines species taxonomic and geographic
information with links to other resources and expertise, it is currently the most comprehensive standardised database of marine introduced species. In addition, WRiMS forms
the basis for a future global early warning system of marine species introductions.
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Samantha Tracy, Julie L. Day, Julianne Renner and Mark Sappington
Human dimensions of aquatic invasive species transport at Lake Mead National Recreation Area (pp 812–827) |
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Since the January 2007 discovery of quagga mussels (Dreissena rostriformis bugensis) at Lake Mead National Recreation Area,
the National Park Service has worked with numerous agencies and partners to prevent further spread of invasive species through inspection
and decontamination of recreational vessels and boater education programs. We applied geographic and demographic analysis techniques
to data collected at inspection and decontamination stations within the park and data from inspection stations across the western United
States to better understand the visitor boating population. Using ArcGIS ESRI Tapestry software and the home zip codes of recreational
boaters whose vessels were inspected within the park, we classified local and non-local boaters into demographic groups with
the goal of developing more targeted educational programs. Demographic results indicate distinctive trends within the boating population
including: higher median incomes, high levels of education, and boat owner median ages in the mid-30s. Economic and behavioral patterns
of Lake Mead boater demographics combined with a synthesis of available research on behavior change in environmental campaign design
demonstrate the need for targeted outreach to increase the effectiveness of aquatic invasive species (AIS) programs and further
reduce AIS transmission risk.
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Jorge E. Ramírez-Albores and Ernesto I. Badano
Alien species as counterpart of a megadiverse country as Mexico (pp 828–845) |
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Improving the knowledge on the distribution and impacts of alien species in poorly studied regions is essential to raise national awareness as well as support effective management
policies. Here we present a systematic review of the current state of knowledge regarding biological invasions in Mexico, providing a list of alien plant and animal species
that can be considered either alien or invasive. Our search in scientific literature comprised a total of 2664 alien species recorded in Mexico, where approximately 36.2%
of alien species were considered invasive, a much higher figure than previous estimates. Most alien species were introduced from the Europe, Asia, and Africa, primarily
for ornamental use, food, or livestock fodder. The current data demonstrate that alien and invasive species continue to enter and spread within Mexico, and it also emphasizes
the necessity and responsibility to develop scientific strategies to minimize the impact of biological invasions and to raise public awareness of the problem. This review
will help fill some gaps in the knowledge about biological invasions in Mexico, where the list of species can serve as a scientific basis for future studies.
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Ernik Yuliana, Yonvitner, Surya Gentha Akmal, Rafialwan A. Subing, Sultan A. Ritonga, Agus Santoso, Antonín Kouba and Jiří Patoka
Import, trade and culture of non-native ornamental crayfish in Java, Indonesia (pp 846–857) |
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The pet trade is known to be one of the main sources of invasive species including freshwater crayfish, which cause socio-economic losses and negative impacts
on native biota in many regions where introduced. Indonesia was identified as the leading supplier of ornamental crayfish globally but the local market has been
neglected even though certain non-native species were reported previously. Based on the survey of pathways and culture of ornamental crayfish in Java, six non-native
species were recorded: Cherax destructor, C. quadricarinatus, C. peknyi, C. snowden, C. warsamsonicus, and P. clarkii.
The latter species originates from North America and serves as a vector of crayfish plague, i.e. a disease lethal for non-North American crayfish species.
Crayfish are cultured both in outdoor and indoor facilities as well as in natural lakes and reservoirs. Harvested crayfish are transported via numerous routes across
most of the island of Java. It is obvious that the local market for ornamental crayfish is well-developed and Jakarta, Surabaya and Yogyakarta were identified
as hotspots of this trade. Further monitoring, detailed analysis of the market and a ban of high-risk P. clarkii are recommended to improve management
and existing legislation.
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A. Simon Ernstsons, Mei-Ying Lin, You Li and Jiri Hulcr
Host associations between xylophagous longhorn beetles (Coleoptera: Cerambycidae) and American commodity tree species from Chinese collection sources (pp 858–872) |
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A small number of longhorn beetle species (Coleoptera: Chrysomeloidea: Cerambycidae) have the potential to become invasive forest pests. International trade in live plants
and wood packaging material are known invasion pathways for longhorn beetles. Once an invasive pest is intercepted in a new region, a rapid pest risk analysis is often needed
to determine the appropriate response. For accurate risk quantification, natural history evidence is necessary. This information is also vital in preventing introduction.
This study gathered insect collection data, especially references to host plants, of xylophagous longhorn beetles from the Institute of Zoology, Chinese Academy of Sciences,
Beijing, China. Beetle associations with three important host groups were investigated: Fagaceae, Citrus spp., and avocado (Persea americana). We performed
a systematic literature review to identify previously documented cerambycidae associated with these plants. Here, we report insect-plant host associations for 39 species
of longhorn beetles based on a review of the literature; 43 interactions were documented, 10 interactions were novel. No host associations were recorded with avocado in China.
This information serves as a foundation for pest risk analysis in determining threats posed by potentially invasive longhorn beetles into new regions.
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Peliyagodage C.D. Perera, Tomasz H. Szymura, Louis de Patoul, Tetiana Sladkovska and Magdalena Szymura
A community resembling semi-natural meadow is as resistant to goldenrod invasion as highly productive commercial grassland (pp 873–885) |
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Alien goldenrods (Solidago and Euthamia) invade improperly managed grasslands causing serious environmental
problems. The general knowledge regarding habitat resistance against invasion does not allow predicting whether species-rich semi-natural
meadows or highly productive artificially sown grasslands are more resistant to invasion by goldenrods. To test the differences
in resistance, an experiment was conducted. A community resembling a semi-natural, species-rich meadow and a commercial
grassland was created in containers in 2018 using seed mixes, with open soil serving as the control. Three goldenrod seedlings
representing particular species (Solidago canadensis L. s.l., S. gigantea Aiton, and
Euthamia graminifolia (L.) Nutt.) were planted in the test containers with the different communites in 2019.
The vegetation was cut once per year during the first and second years of the experiment. In September of the third year,
the number of goldenrod ramets, the height of the tallest goldenrod ramet, and the flowering stage were measured and assessed.
In addition, the dry biomass of goldenrods and accompanying species were weighed. The results showed no significant differences
between total biomass production of the examined communities, except for E. graminifolia, for which species-rich meadow
produced more biomass than the commercial grassland and control. Both communities strongly reduced ramet numbers and height
and goldenrod biomass production compared to the control. No differences were found between these two vegetation types,
except for the flowering stage of S. canadensis and E. graminifolia, which could not produce seeds
in the species-rich meadow community. The results suggest that semi-natural, species-rich meadows are reasonable alternatives
to species-poor commercial grasslands to control goldenrod invasion.
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Sri Rahayu, Rahman Gilang Pratama, Muhammad Ali Imron, Januar Mahmud and Widyanto Dwi Nugroho
The occurrence of gummosis on invasive Acacia decurrens after Mount Merapi eruption in Yogyakarta, Indonesia (pp 886–900) |
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Gummosis on Acacia decurrens, an invasive tree species that was established in Merapi Volcano National Park (MVNP)
after the eruption of the Mount Merapi volcano in 2010, was studied to i) identify the causal organism of the disease,
ii) analyze the disease symptoms, iii) understand the spatio-temporal distribution of gummosis in the tree population
and iv) examine how the disease affects the anatomy of tree wood. Pathological, morphological and molecular assessments
were used in this study. Ceratocystis fimbriata was found associated with gummosis in the affected trees.
The disease spread was probably aided by an ambrosia beetle, Euwallacea sp., which bores holes in the stem.
The number of parenchyma cells in infected stems was significantly higher than in healthy stems, which apparently facilitated
water and nutrition transport within trees, helping them to grow normally despite serious gummosis. The disease is noted
to spread from the base of the trees, where the ambrosia beetle bores holes first, to the upper part.
The management of invasion by A. decurrens in the MVNP area poses a serious challenge due its success as an invader
in the volcano-impacted area and the threat of the gummosis pathogen spreading to other species, both of which will affect
the regeneration and establishment of native species and recovery of the ecosystem.
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Amy A. Yackel Adams, Patrick D. Barnhart, Gordon H. Rodda, Eric T. Hileman, Melia G. Nafus and Robert N. Reed
Can we prove that an undetected species is absent? Evaluating whether brown treesnakes are established on the island of Saipan using surveillance and expert opinion (pp 901–926) |
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Detection of invasive species and decisions centered around early detection and rapid response (EDRR) are notorious challenges for decision makers. Detection probability is low
for cryptic species, resources are limited, and ecological harm (especially for island ecosystems) can result from failure to remove invasive species due to inadequate or delayed
surveillance efforts. Due to the proximity to the U.S. territory of Guam and inter-island traffic, the Commonwealth of the Northern Mariana Islands (CNMI) is at high risk of colonization
by the invasive and cryptic brown treesnake (Boiga irregularis; BTS). There have been numerous reports of snakes and 7 confirmed specimens secured at ports of entry on the island
of Saipan in the CNMI over the last four decades, raising the possibility that a population might be established. Establishment of BTS on Saipan is a major concern, as evidenced
by the ecological and economic disruption that occurred on Guam. We evaluated the possibility of a small localized population on Saipan using evidence from surveillance efforts in 1999,
2007, 2009, 2016, and 2018, and from results of expert assessment of the credibility of non-confirmed reports of snakes for the period 1982–2013. For active surveillance efforts,
we use a Poisson-based model to estimate the 95% probability of at least one snake being detected at a stated density given the level of sampling effort and detection probability.
Based on this collective evidence we conclude there is a low probability that Saipan currently has an incipient population of BTS. However, with the continued presence of BTS on Guam,
continuing commercial and military transportation in the region, and relief shipments responding to increased storm intensity, Saipan remains highly vulnerable to accidental introductions.
Effective surveillance remains a crucial element for detection of any species, but this may be particularly true for a cryptic snake that is difficult to control once established.
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Diane L. Waller, Lynn Bartsch, Michelle R. Bartsch, Matthew Meulemans, Todd Severson and Thomas J. Zolper
Use of carbon dioxide to prevent zebra mussel (Dreissena polymorpha) settlement and effects on native mussels (Order Unionoida) and benthic communities (pp 927–951) |
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We determined the efficacy of carbon dioxide (CO2) for preventing larval (veliger) settlement of the invasive zebra mussel (Dreissena polymorpha)
and compared the response of native juvenile mussels and macroinvertebrate and periphyton communities to hypercapnia. A microcosm system of control
(ambient Camb) and CO2 treatments [low partial pressure of carbon dioxide,
PCO2 (Clow) = 35,094 µatm, and high PCO2
(Chigh) = 66,685 µatm)] was supplied with river water for 11 weeks. We measured zebra mussel settlement, juvenile native mussel
(Lampsilis cardium and L. siliquoidea) growth and condition, and macroinvertebrate and periphyton community composition. Zebra mussels settled in all
Camb tanks (n = 4) from early July through August compared to one mussel in a CO2 treatment tank
over the same period. Native mussel growth, tissue condition, and shell condition were reduced in CO2, particularly in the highest treatment.
Benthic biomass (excluding zebra mussels) was similar in Camb and Clow but was reduced in
Chigh. Macroinvertebrate community composition differed among treatments due to greater abundance of Chironomidae
in Clow and Oligochaeata in Chigh. Periphyton abundance and richness increased in both
CO2 treatments and was driven by increases in Cyanobacteria, Bacillariophyta, and Chlorophyta. Our results indicate that efficacious levels
of CO2 (~ 35,000 µatm PCO2) for reducing biofouling by dreissenids
are tolerable to most freshwater benthic taxa. Chronic elevated CO2 infusion (> 35,000 µatm PCO2)
may reduce native mussel growth and condition and alter benthic invertebrate and periphyton community composition. Further refinement of CO2
application strategies is needed to determine minimum effective dose and duration to prevent dreissenid settlement and minimize effects on nontarget organisms.
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Hisham A. Abdelrahman, Rebecca L. Gibson, Kaelyn J. Fogelman, Aaron R. Cupp, Ann L. Allert and James A. Stoecke
Evaluation of dissolved carbon dioxide to stimulate emergence of red swamp crayfish Procambarus clarkii (Decapoda: Cambaridae) from infested ponds (pp 952–974) |
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Invasive crayfish have adverse effects on habitats and native species. Control of invasive crayfish populations is a major challenge
facing natural resource managers. This study evaluated the effectiveness and optimal conditions for the control agent
carbon dioxide (CO2), which can be diffused into water to facilitate capture of red swamp crayfish
(Procambarus clarkii; RSC). The efficacy of CO2 shows promise in its use for a variety
of invasive aquatic species. Here, we evaluate CO2’s ability to stimulate movements towards
the shoreline and/or induce complete terrestrial emergence from outdoor ponds. Twelve pond trials were conducted using three,
0.02-ha experimental ponds at Auburn University, Alabama, USA. Silt fencing was installed on dry land around the perimeter of each pond
with the lower 0.3 m of fencing accordion-folded to provide shelter and a collection point for emerging crayfish. Each pond was stocked
with 100 RSC before testing. Experimental treatment ponds were then injected with gaseous CO2
using porous air diffusers, whereas control ponds (C ponds) received no CO2. Multiple water quality
parameters were monitored hourly. Three independent treatment scenarios with CO2 diffusion were
crayfish captured at the end of trial only (F: final), crayfish captured hourly (H: hourly), and incorporation of continuous inflow
of fresh water at a flow rate of 0.2 L/s into the central catch basin to serve as a refuge with crayfish captured hourly (R: refuge).
In control ponds, crayfish were captured at the end of trial only. In F ponds, CO2 diffusion
for approximately five hours caused a mean of 12% of total crayfish to emerge from the water. However, capture efficiency was increased
to a mean of 45% of total crayfish by increasing collection frequency to every hour and netting submerged crayfish near the water edge
in addition to capturing terrestrially emerged crayfish. Presence of a freshwater inflow reduced capture efficiency in R ponds relative
to H ponds. Odds of capturing crayfish increased with increasing water temperature, CO2
concentration, crayfish mass, and with decreasing pH. Based on results, we provide a set of predictive equations as well as interactive
calculators to help natural resource managers explore several environmental and treatment-related scenarios that predict changes
in capture probability in small research ponds. Carbon dioxide shows promises as a tool to increase capture rate of RSC. It is not likely
to be 100% effective by itself, but could be a useful component of an integrated management strategy.
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Jake T. Kvistad, Tracy L. Galarowicz, David F. Clapp, W. Lindsay Chadderton, Andrew J. Tucker and Matthew E. Herbert
An evaluation of three trap designs for invasive rusty crayfish (Faxonius rusticus) suppression on critical fish spawning habitat in northern Lake Michigan (pp 975–996) |
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High densities of invasive rusty crayfish on critical spawning reefs present a potential impediment to the recovery of native fish in the Laurentian Great Lakes.
Suppression of rusty crayfish on spawning reefs to protect fall spawning native fishes in the Great Lakes is hampered by regular storm events and ambient weather
conditions, limiting the number of practical days traps can be checked, cleared, and re-baited. The Gee minnow trap design is the most common gear for sampling
and managing crayfish, yet design constraints of the standard Gee minnow trap manifest as tradeoffs between capture efficiency and retention for users. In this study,
we compared catch rates from a semi-controlled field experiment and escapement probabilities from laboratory controlled trials for a Gee minnow trap, a modified
Gee minnow trap with intention to reduce escapement, and an experimental flat-bottomed pyramid design which showed potential promise during prototype-stage development.
Bayesian parameter estimation of generalized linear models applied to catch data suggested that standard Gee minnow traps performed at least as well and often better
than both novel trap designs in catch rate and escapement probability. Escapement during laboratory controlled trials was high for all trap designs, demonstrating
that retention of trapped individuals is a persistent problem for crayfish monitoring and management. We conclude from our data that standard Gee minnow traps are
a sensible gear choice for monitoring and/or potential suppression efforts for invasive rusty crayfish on nearshore spawning reefs in the Great Lakes. However,
modifications to its design to improve retention should yet be pursued.
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Yasufumi Fujimoto, Kiyotaka Takahashi, Kentaro Shindo, Takeshi Fujiwara, Koichi Arita, Kenji Saitoh and Tetsuo Shimada
Success in population control of the invasive largemouth bass Micropterus salmoides through removal at spawning sites in a Japanese shallow lake (pp 997–1011) |
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The control of invasive species is of major importance for ecological conservation, and there is a need for more effective techniques and approaches to control
these species, especially in open habitats. Two types of activities were conducted to control the population of largemouth bass (Micropterus salmoides)
in Lake Izunuma-Uchinuma, Japan. The first activity was a lake wide catch using set nets deployed all along the lakeshore beginning in 2001. The second activity,
beginning in 2004, focused on catches during the spawning season over spawning sites, distributed along lakeshore segments with sandy substrates. The efforts
of both activities were similar (involving about 140 people/year). From 2001 to 2003, the catch per unit of fishing effort (CPUE) of largemouth bass
using set nets increased; however, CPUE decreased dramatically after catches at the spawning sites started. The numbers of nests spawned, larvae, and adults
of largemouth bass also decreased after the start of spawning site catches. In 2010, the CPUE of other fish species, whose numbers had decreased due to predation
by largemouth bass, recovered to the same number as before the expansion of largemouth bass. Capturing largemouth bass at the spawning sites
was an effective approach to controlling this species and conserving fish communities in the lake.
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Adel Kacimi, Abderrahmane Bouda, Michael Sievers, Bilel Bensari, Fouzia Houma, Lamri Nacef and Nour El Islam Bachari
Modeling the risk of introducing non-indigenous species through ship hull biofouling: case study of Arzew port (Algeria) (pp 1012–1036) |
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Biofouling of ship hulls is one of the most important vectors for the transfer of aquatic invasive species.
These species cause widespread impacts to native environments and ecological communities, in addition to imposing financial costs for industry.
Targeted surveillance and effective adaptive management require knowledge on the likelihood of new introductions of non-indigenous species (NIS).
We develop a model of the likelihood of introduction and invasion of NIS for the port of Arzew (Algeria), based on the length of stay of vessels in the ports of call,
the latitude of these ports, the geographical distance from the port of Arzew, ship’s speed, effectiveness of the antifouling system and antifouling strategy
used in port of origin. We identified areas that represent a source of high risk species invasion, according to the environmental similarity of the ports of origin
with the Arzew port using the Mahalanobis distance. We show that over one year, 738 trips have been made at the port of Arzew, inflicting a very high risk of invasion,
in particular from six coastal ecoregions, (the Western Mediterranean ecoregion, the Northern and Central Red Sea, the South European Atlantic Shelf,
the Ionian Sea ecoregion, the North Sea, and the Aegean Sea). These results can be used for invasive species management purposes, such as:
the application of specific regulations to high-risk vessels and ports in order to minimize the transfer of these species.
The methods and models developed here are transferable to any region around the world with similar data availability.
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