Decadienal afforestation and risks to montane grassland amphibians in the Udzungwa Plateau, Tanzania

Human modification of the environment has drastically changed ecosystems around globe. While forest-loss (deforestation) been well studied for its effects on ecosystems, afforestation also major impacts. The Udzungwa Plateau in Tanzania is naturally a mix forests and grasslands. However, non-native pine plantations have recently increased area displacing native grasslands montane plateau. In this study, we explored land use change amphibian communities by comparing surveys before were introduced (~2000) after (2017–2019). To put these into wider context across plateau to distinguish local population loss compared plateau-wide extinctions, sample diversity at new sampling locations with multiple through time. We then assessed landscape remotely sensed data ground surveys. Amphibian encounter found approximately same species all locations, but extinctions appear likely. Remaining amphibians be limited small refugia non-pine wetlands. Approximately half (45%) distributional ranges (<72,000 km2) are described as habitat specialists IUCN Red List. Monitoring plantation growth using remote sensing techniques suggested only extensions between 2000 2013–2016, pines (<3 years old) throughout almost areas identified satellite imagery. Our study highlights plight narrowing biome African continent calls more research impact natural communities. Abstract Swahili available online material. Shughuli za kibinadamu zimesababisha mababadiliko makubwa ya mifumo ikolojia kote ulimwenguni. Ingawa tafiti nyingi zaidi zimefanyika kuhusu athari uharibifu wa misitu utokanao na ukataji miti, upandaji miti maeneo yasiyo pia una kubwa kwenye ikolojia. Uwanda juu milima nchini kwa asili unaundwa uoto pamoja sehemu wazi zilizotawaliwa nyasi. Hata hivyo, mashamba isiyo aina misindano mikaratusi yameongezeka katika eneo hili la uwanda siku hivi karibuni, haswa ambayo kiasili yalikua Utafiti huu, ulijikita kuchunguza mabadiliko matumizi ardhi viumbe amfibia, kulinganisha taarifa zaokwenye haya kabla (mwaka 2000) baada (kati mwaka 2017–2019). Ili kuweka hizi amfibia muktadha mpana juu, ili kuwezesha kutofautisha madhara dogo, kutoweka vyura pana nyanda tulilinganisha mapya tuliyochunguza karibuni kujumuisha zote zilizofanyika huu kutathmini kuchakata kutoka satelaiti. idadi spishi ilionekana kubaki vilevile uwanda, uwezekano baadhi walipokua wakipatikana hapo awali umekuwa dhahiri. Amfibia waliosalia wanaonekana kuwepo tu viraka vidogo oevu ambavyo bado havina misindano. Takriban nusu zilizopatikana ni zile zenye safu ndogo sana usambaaji zinatambulika shirika kimataifa uhifadhi bionuai (IUCN) kuwa zinapendelea kuishi makazi fulani pekee. Ufuatiliaji ongezeko satelaiti ulionesha dogo kati hadi lakini uhakiki midogo (umri chini miaka 3) takribani yote yaliyotambuliwa kama nyasi picha wetu unatoa masaibu yanayokumba muhimu kiikolojia linaloendelea kupotea haraka barani Afrika kutoa wito utafiti kina mazingira. Tropical unique ecosystem consisting cool, high-elevation Africa, South America, India, Southeast Asia typically surrounded mid- lower-elevation tropical (www.worldwildlife.org). hold significant biodiversity, endemic that (Bond & Parr, 2010). Like other experiencing high levels from human activities, open stable rains conducive conversion agricultural fields tree (Arasumani et al., 2018; Farley, 2007; Hermann 2016). As habitats converted, grassland may increasingly become vulnerable extinction. One particularly prevalent form afforestation: act or process establishing forest especially not previously forested. Afforestation rising world fast-growing, planting encouraged governments NGOs environmental societal benefits (e.g., timber production, flood regulation, carbon sequestration; Bond, 2016; Bond 2019; Di Sacco 2021; Parr 2014). Non-native trees preferentially planted due their exceptionally rates an increasing demand wood products (Ngegba 2001). negative impacts such water consumption, decreased quality, biodiversity loss, soil quality food web disruption recognized (Allan 1997; Armstrong van Hensbergen, 1999; Iezzi 2020; Principe 2015). These can impactful ecosystem, they affect yield catchments, chemistry ways suitable wildlife (Berthrong 2009; Burraco Schwärzel 2020). both Eucalyptus common world, (genus Pinus) dominant (>78%; Ngaga, 2011). unknown (Rundel Most directly, impacted fragmentation, vegetation transformed monocultures pine. Grassland often assumed generalist species, tolerant encroachment than see treatment forest-associated resilience landcover types including grasslands; Thompson assumption rarely tested. Studies indicate 1998; Zaloumis Thus, without sufficient intact recolonizations, lead total extinctions. subtropical regions, ranging Ethiopian Montane Moorlands North, Drakensberg region South, southern Malawi East, Jos Nigeria West (https://www.oneearth.org/bioregions/). distinct surrounding forested areas. Endemism thought derived ancient emergence higher elevations isolated submontane (Burgess Carbutt, Lawson 2015; Menegon 2006; Perera 2011; Rossi 2010; Tadele East (Figure 1) part Eastern Arc Mountains Afromontane hotspot (Conservation International). system block-faulted mountains endemism separated savanna lowlands. Mountain block highest number any mountain chain. This correlated larger size (~10,000 elevational range (300 m 2800 m, most hills 1200 a.s.l), which encompasses many grassland-forest mosaic. persisted thousands (~13,000 years; Finch Marchant, 2011), forest, upper forest. Forested under varying protection, over 27 reserves, national park, two nature village privately owned 1). Grasslands outside protected fall within “gaps Tanzania's Protected Area Network” (Rodgers, 1998). Worryingly, given little attention surveys, thus accurate estimates hampered incomplete inventories baselines. 2004–2005, unprotected 2) having extensive cultivation (some farms valley bottoms slopes) few cows (Rossi Lacking growing population, experienced rapid increase extent (Brink Meng Landscape fueled (with 26% 24 1988 2012; Kangalawe, 2018) recent programs encouraging non-industrial private forestry (NIPF; small-scale planting) ease pressures wood. NIPF plantings primarily accomplished donor-funded incentive schemes, Hifadhi Mazingira (1990–2002), Private Forestry Programme (2014 onward), Development Trust (2013 onward) (summarized Koskinen 2019). Such tree-planting people plant trees, lacked restrictions guidance where did seekt avoid plantations. Before push, government Sao Hill Forest Plantation, ~57,000 Ha) began early 1930s, corporate Green Resources Ltd, GRL, 12,000 smallholders (individually/family plots, usually <1 begav (Kangalawe, Kimambo Pines (Pinus patula) make up 67% (Arvola Smallholder largest proportion 210,000–250,000 ha (64%; Arvola 2019), supported (PFP) Tanzania. large holder Limited (GRL), “leading plantation, offset renewable energy company eastern Africa”. GRL holds long-term lease beginning 2006 projects. existed highlands Southern 100 years, “smallholder strongly emerged Highlands since 2007” Programme, 2017). still poorly known. A wide variety animals 1996, Graham 2017; 2015), different animal groups could used indicators type ecosystem. Amphibians serve reliance aquatic terrestrial landscapes sensitivity (Cushman, Grant Hof Lips, assess plantations, compare lists known Gendawaki (Gendvaki) Valley (Menegon Salvidio, 2005; 2010) 2017 2019 (this study). fieldwork sought same, previous sites much possible. Upon visiting surveyed noted if was unchanged (still grasslands), shifted agriculture presence (or lack thereof, absent) gain sense how scale. changes abundance view distributions (population extinctions), first searched literature encounters (primary result 1929–1930 surveys; Loveridge collections Harvard University Herpetology database). demarcated Dabaga, Bomalang'ombe, Mapanda villages Reserve 2), listed “swampy” Tanzanian survey maps. See al. (2010) descriptions area. features time imagery estimate cover onward trends Plateau. Two re-evaluated modern nomenclature resolve “unknown species” best possible those reported works. involved contacting experts each current nomenclature, incorporating genetic studies geographic newly named Phrynobatrachus discogularis), consulting Species World website (Frost, 2023). name employ currently Xenopus victorianus, about consulted expert taxon (B. Evans, McMaster University). Photographs determine samples corresponded to. 1929/1930 Africa (Museum Comparative Zoology, herpetology database; Loveridge, 1933). our knowledge, no full completed except extended Cavada Werema 2012), explored. Specifically, order identify non-exhaustive chance encounters, formal informal investigations made Informal inquiries writing vertebrate biologists who worked past decades specimens collected conducted. Formal searching Google Scholar combinations keywords “amphibian, Udzungwa, grasslands, frog, caecilian, survey.” http://vertnet.org/ museum (“in circle map” search feature). All localities towns excluded. Collection (2006) one revisited document potential took place during long rainy season (described below), additional days August (2006). Further, (see below) broader spatial representation periods: December February 2019, corresponding traditional “long period” night flashlights guided calling individuals triangulated. Both spent driving waterlogged (Mapanda sites) arial photos containing (Mlama), met continuous mature amphibians. included wetland nor, heard. simply recorded longer being sites. Only successfully sampled (Gendawaki Hill) effort. 2017, four nights 19:30–00:00 day (4.5 h × 3 4 = 54 hours) Kiolela, Gendawaki, Ng'ang'ange, New Dabaga 2a, blue dots circle). Kiolela Bomalang'ombe day, second third days, fourth day. Heavy lighter following days. three targeting remaining wetlands Pine Plantation adjacent military training 2a,d). Light occurred Total effort 40.5 hours days). Combined 94.5 h. addition active searching, drift fence (20 meters) five 20-L buckets plastic sheeting set flooded checked morning 2 “Mapanda” heard, observations added support officers grassland-wetlands governmental blocks, despite earlier captured photographed field record coloration. Voucher euthanized applying overdose benzocaine forehead, preserved 70% alcohol. accordance ethics guidelines established institutions authors (including Cincinnati [IACUC 21-04-21-02; LPL]), Natural History Museum London, approved Wildlife Research Institute (TAWIRI). List assessment (IUCN, 2022) provide qualitative less extinction tend ecology species. Extent occurrence (EOO; contained shortest imaginary boundary drawn encompass known, inferred, projected present excluding cases vagrancy) obtained List, when available. When available, polygons sources Channing Rödel, 2019) approximations (increased include already documented). Distribution showed clear bimodality (species <100,000 km2 >500,000 km2; Table therefore discretized acknowledge expected harbor cryptic reflect lineages, thereby overestimated sizes Bittencourt-Silva Habitat preference information compiled independent marker specialist besides (which necessarily), focusing phrases “many types” “adapts land” ecology. estimated expansion ways: published, (both plantation-specific non-specific cover) published “plantations (2019) (maps dating 2013–2016) Global Change map (Hansen 2013) 2000. datasets resolution 1 arc-second per pixel, 30 meters pixel equator, difference category ~16 years. incentives focused turning encourage turnover Therefore, dataset “trees” considered Maryland establish (natural plantation) extant Areas “plantation growth” period calculated global map. raster file created multi-sensor image stacks Landsat, Sentinel, elevation slope layers datafiles 2013 2016. Age classes (0–3, 3–7, 8+-year-old growth) taken (2017) (2019). states youngest age class (trees 0–3 likely underestimate hardest remotely. Due young area, undercounted (and addressed “ground truthing plantations” section below). modified >10% recommended Schmitt (2009). designed incorporate tree-free landscape. Datasets clipped ESRI Arcmap (version 10.8.1) shapefile Platts (2011). change, maps (Land Cover 2010, Scheme I; ArcGIS.com) 2010 relative proportions (forestland, grassland, cropland, wetland, settlement). 2020 (ArcGIS.com) though “forestland/trees” confidence classifications rasters trimmed Pixels “cloud”, “shadow”, “other excluded, percentages values had numbers categories while later not. free (native plantations), categorized historical (1989 Ordinance 1:50,000), (Tanzania Land Use Map 2000–2010, ESRI), Earth (2017 imagery) visited Sites either (primarily maize family mixed crops), encountered clear, neat rows implying intentional rather invasive expansion. provides under-reported uses times too adequately capture. Literature searches (Vertnet.org) revealed collecting trips presumed times, manner. include: Arthur (six dates recorded, collection span months), Arne Schiøtz 1971 (two consecutive days), Westergaard 1997 non-consecutive Hendrik Müller Joanna Larson 2009 (6 recorded). non-comprehensive possiblity Loveridge. (2009) larval stages. Based data, tadpoles Hyperolius pictus, H. substriatus, Ptychadena uzungwensis. (1929–1930) appears broadly his along Schiotz (1971) howelli (previously nasutus acuticeps; 2013), viridiflavus goetzei, considering fully Likewise, (1997) (Hyperolius pseudargus Leptopelis cf. grandiceps, formerly L. barbouri; Gvoždík 2014) seen therefore, think nearby instead Another survey, aimed detecting chytrid pathogen (Batrachochytrium dendrobatidis; Bd) (sampling 2004–2005; Moyer Weldon, 2006), contains site (Maganga) water-associated former (terrestrial surveyed). Frogs recovered there mainly higher-elevation minutissimus, pseudargus) some widespread victorianus). converted dairy coffee farm comparison Nineteen (Table list similar (2010), spp.” older names updated nomenclature. directly comparable, designated Hill. regional comparisons direct (old 10 according workers), grass understory completely gone covered thick blanket needles. No heard near wetland-associated would present. very (anecdotally ~3–5 old), saplings, otherwise so heavily draining wetland) it deemed Some proved difficult classify species-level based morphology alone. particular understood able certainty represented light revisions DNA evidence. Across region, encountered. Eleven 72,000 below There break (small ranges) (>500,000 km2). summarizing requirements smaller distribution characteristics imply flexibility “Montane endemic”) unlike 13 km2), notes “Tolerates anthropogenic habitats” “ability exist habitats”. Using calculating eucalyptus 760.8 (“2013–2016 dataset”). 2000, 698 km2, 62.8 2013–2016 dataset. documents “moderate mature” (>8 years), successful recognizing category. According (2019), (0–3 years) counted accurately classify, intermediate (4–7