A Review of the Engineering Role of Burrowing Animals: Implication of Chinese Pangolin as an Ecosystem Engineer

Authors

  • Song Sun Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin, 150040, China;Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou, 510520, China
  • Hongliang Dou Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou, 510520, China
  • Shichao Wei Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou, 510520, China
  • Yani Fang Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, M2J4A6, Canada
  • Zexu Long Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin, 150040, China
  • Jiao Wang Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou, 510520, China
  • Fuyu An Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry,Guangzhou, 510520, China
  • Jinqian Xu Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry,Guangzhou, 510520, China
  • Tingting Xue Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin, 150040, China;Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry, Guangzhou, 510520, China
  • Huangjie Qiu Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry,Guangzhou, 510520, China
  • Yan Hua Guangdong Provincial Key Laboratory of Silviculture, Protection and Utilization, Guangdong Academy of Forestry,Guangzhou, 510520, China
  • Guangshun Jiang Feline Research Center of National Forestry and Grassland Administration, College of Wildlife and Natural Protected Area, Northeast Forestry University, Harbin, 150040, China

DOI:

https://doi.org/10.30564/jzr.v3i3.3102

Abstract

Ecosystem engineers are organisms that alter the distribution of resources in the environment by creating, modifying, maintaining and/or destroying the habitat. They can affect the structure and function of the whole ecosystem furthermore. Burrowing engineers are an important group in ecosystem engineers as they play a critical role in soil translocation and habitat creation in various types of environment.However, few researchers have systematically summarized and analyzed the studies of burrowing engineers. We reviewing the existing ecological studies of burrowing engineer about their interaction with habitat through five directions: (1) soil turnover; (2)changing soil physicochemical properties; (3) changing plant community structure; (4) providing limited resources for commensal animals;and/or (5) affecting animal communities. The Chinese pangolin (Manis pentadactyla) is a typical example of burrowing mammals, in part (5), we focus on the interspecific relationships among burrow commensal species of Chinese pangolin. The engineering effects vary with environmental gradient, literature indicates that burrowing engineer play a stronger role in habitat transformation in the tropical and subtropical areas.The most common experiment method is comparative measurements (include different spatial and temporal scale),manipulative experiment is relatively few. We found that most of the engineering effects had positive feedback to the local ecosystem, increased plant abundance and resilience, increased biodiversity and consequently improved ecosystem functioning. With the global background of dramatic climate change and biodiversity loss in recent decades, we recommend future studies should improving knowledge of long-term engineering effects on population scale and landscape scale, exploring ecological cascades through trophic and engineering pathways, to better understand the attribute of the burrowing behavior of engineers to restore ecosystems and habitat creation. The review is presented as an aid to systematically expound the engineering effect of burrowing animals in the ecosystem, and provided new ideas and advice for planning and implementing conservation management.

Keywords:

Burrowing engineer, Burrow commensal species, Chinese pangolin, Ecosystem engineer, Habitat modification, Biodiversity

References

[1] Jones, C.G. Lawton, J.H. Shachak, M. (1994),“Organisms as ecosystem engineers”, Oikos., 69,373-386.

[2] Jones, C.G. Lawton, J.H. Shachak, M. (1996),“Positive and negative effects of organisms as physical ecosystem engineers”, Ecol., 78, 1946-1957.

[3] Coggan, N.V. Hayward, M.W. Gibb, H. (2018),“A global database and "state of the field" review of research into ecosystem engineering by land animals”, J. Anim. Ecol., 87(4), 974-994.

[4] Bragg, C.J. Donaldson, J.D. Ryan, P.G. (2005),“Density of Cape porcupines in a semi-arid environment and their impact on soil turnover and related ecosystem processes”, J. Arid. Environ., 61,261-275.

[5] Desbiez, A.L.J. and Kluyber, D. (2013), “The role of giant armadillos (Priodontes maximus) as physical ecosystem engineers”, Biotropica., 45, 537-540.

[6] Reichman, O.J. Smith, S.C. (1990), “Burrows and burrowing behaviour by mammals”, In:Genoways,H.H. (Ed.), Curr. Mammal., 2, 197-244.

[7] Kinlaw, A. (1999), “A review of burrowing by semifossorial vertebrates in arid environments”, J.Arid.Environ., 41, 127-145.

[8] Whittington-Jones, G.M. (2007), “The role of aardvarks (Orycteropus afer) as ecosystem engineers in arid and semi-arid landscapes of South Africa”.

[9] Ecological Society of America. ScienceDaily, 31 January 2008, "Ecosystem Engineers: Elephant Eating Habits Influence Lizard Habitat Choices”,ScienceDaily.

[10] Haussmann, N.S. (2017), “Soil movement by burrowing mammals: A review comparing excavation size and rate to body mass of excavators”, Prog.Phys. Geogr: Earth and Environment., 41(1),29-45.

[11] Sawyer, C. Brinkman, D. Walker, V. Covington,T. Stienstraw, E. (2012), “The zoogeomorphic characteristics of burrows and burrowing by ninebanded armadillos (Dasypus novemcinctus)”,Geomorphology., s 157-158, 122-130.

[12] Eriksson, B. Eldridge, D. (2014), “Surface destabilisation by the invasive burrowing engineer Mus musculus on a sub-Antarctic island”,Geomorphology., 223, 61-66.

[13] Borchard, P. Eldridge, D.J. (2011), “The geomorphic signature of bare-nosed wombats (Vombatus ursinus) and cattle (Bos taurus) in an agricultural riparian ecosystem”, Geomorphology., 130, 365-373.

[14] Coombes, M.A. Viles, H.A. (2015), “Population-level zoogeomorphology: the case of the Eurasian badger (Meles Meles L.)”, Phy. Geo., 36, 215-238.

[15] Garkaklis, M.J. Bradley, J.S. Wooller, R.D. (2004),“Digging and soil turnover by a mycophagous marsupial”, J. Arid. Environ., 56, 569-578.

[16] Casas-Criville, A. (2005), “The European bee-eater (Merops apiaster) as an ecosystem engineer in arid environments”, J. Arid. Environ., 60, 227-238.

[17] Valentine, L.E. Anderson, A. Hardy, G.E.S.J.Fleming, P.A. (2013), “Foraging activity by the southern brown bandicoot (Isoodon obesulus) as a mechanism for soil turnover”, Aust. J. Zool., 60,419-423.

[18] Halstead, L.M. Sutherland, D.R. Valentine, L.E.Rendall, A.R. Coetsee, A.L. Ritchie, E.G. (2020),“Digging up the dirt: Quantifying the effects on soil of a translocated ecosystem engineer”,Austral. Ecol.,45(1), 97-108.

[19] Bancroft, W.J. Hill, D. Roberts, J. (2004), “A new method for calculating volume of excavated burrows:The geomorphic impact of Wedge-Tailed Shearwater burrows on Rottnest Island”, Func. Eco.,18, 752-759.

[20] Mallen-Cooper, M. Nakagawa, S. Eldridge, D.J.(2019), “Global meta-analysis of soil-disturbing vertebrates reveals strong effects on ecosystem patterns and processes”, Global. Ecol. Biogeogr., 28.

[21] Louw., M. Haussmann., N.C, le R., P.C. (2019),“Testing for consistency in the impacts of a burrowing ecosystem engineer on soil and vegetation characteristics across biomes”, Sci. Rep., 9,19355.

[22] Fleming, P.A. Anderson, H. Prendergast, A.S. Bretz,M.R. Valentine, L.E. Hardy, G.E.S. (2013),“Is the loss of Australian digging mammals contributing to a deterioration in ecosystem function”? Mamm. Rev.,44, 2.

[23] Tania, D.A. Olivier, B. François, M. Adeline, B.Erick, P. Thierry, D. (2020), Harvester ants as ecological engineers for Mediterranean grassland restoration: Impacts on soil and vegetation”, Biol.Conserv., 245, 108547.

[24] Qiu, D. Cui, B. Yan, J. Ma, X. Ning, Z. Wang, F. Sui,H. (2019), “Effect of burrowing crabs on retention and accumulation of soil carbon and nitrogen in an intertidal salt marsh”, J. Sea. Res., 154,101808.

[25] Davies, G.T.O. Kirkpatrick, J.B. Cameron, Z.E.Carver, S. Johnson, C.N. (2019), “Ecosystem engineering by digging mammals: effects on soil fertility and condition in Tasmanian temperate woodland”, Royal. Soc. Open. Sci., 6, 180621.

[26] Qin, Y. Chen, J. Yi, S. (2015), “Plateau pikas burrowing activity accelerates ecosystem carbon emission from alpine grassland on the QinghaiTibetan Plateau”, Ecol. Eng., 84,287-291.

[27] Kinlaw, A. Grasmueck, M. (2012), “Evidence for and geomorphologic consequences of a reptilian ecosystem engineer: The burrowing cascade initiated by the Gopher Tortoise”, Geomorphology., 157,108-121.

[28] Ewacha, M.V.A. Kaapehi, C. Waterman, J.M. Roth,J.D. (2016), “Cape ground squirrels as ecosystem engineers: Modifying habitat for plants, small mammals and beetles in Namib Desert grasslands’,Afr. J. Ecol., 54, 68-75.

[29] Burbidge, A.A. Short, J. Fuller, P.J. (2007), “Relict Bettongia lesueur warrens in Western Australian deserts”, Aust. Zool., 34, 97-103.

[30] Kerley, G. Whitford, W. Kay, F. (2004), “Effects of pocket gophers on desert soils and vegetation”, J.Arid. Environ., 58, 155-166.

[31] Dundas, S.J. Hopkins, A.J.M. Ruthrof, K.X. Tay, N.E.Burgess, T.I. Hardy, G.E.S.J. Fleming, P.A.(2018),“Digging mammals contribute to rhizosphere fungal community composition and seedling growth”,Biodivers. Conserv., 27.

[32] Ballová, Z. Pekárik, L. Píš, V. Sibik, J. (2019), “How much do ecosystem engineers contribute to landscape evolution? A case study on Tatra marmots”. Catena.,182.

[33] Kämpfer, S., Fartmann, T., 2019. Breeding populations of a declining farmland bird are dependent on a burrowing, herbivorous ecosystem engineer. Ecol Eng. 140, 105592.

[34] Malizia, B.A. Kittlein, M.J. Busch, C. (2000),“Influence of the subterranean herbivorous rodent Ctenomys talarum on vegetation and soil”, Z.Saugetierkunde., 65: 172-182.

[35] Almeida, T.D. Blight, O. Mesleard, F. Bulot, A.Provost, E. (2020), “Harvester ants as ecological engineers for Mediterranean grassland restoration:Impacts on soil and vegetation”, Biol. Conserv., 245,108547.

[36] Wright, J.P. Flecker, A.S. Jones, C.G. (2003), “Local vs. landscape controls on plant species richness in beaver meadows”, Eco., 84(12), 3162-3173.

[37] Bartz, S.E. Drickamer, L.C. Kearsley, M.J.C. (2007),“Response of plant and rodent communities to removal of prairie dogs (Cynomys gunnisoni) in Arizona”, J. Arid. Environ., 68, 422-437.

[38] Valentine, L.E. Bretz, M. Ruthrof, K.X. Fisher, R.Hardy, G. Fleming, P. (2016), “Scratching beneath the surface: Bandicoot bioturbation contributes to ecosystem processes”, Austral. Ecol., 42.

[39] Garkaklis, M.J. Bradley, J.S. Wooller, R.D. (2000),“Digging by vertebrates as an activity promoting the development of water-repellent patches in subsurface soil”, J. Arid. Environ., 45, 35-42.

[40] Garkaklis, M.J. Bradley, J.S. Wooller, R.D. (2003),“The relationship between animal foraging and nutrient patchiness in south-west Australian woodlands”, Aust. J. Soil. Res., 41,665-673.

[41] Eldridge, D.J. and Mensinga, A. (2007), “Foraging pits of the short-beaked echidna (Tachyglossus aculeatus) as small-scale patches in a semi-arid Australian box woodland”, Soil. Biol. Biochem., 39,1055-65.

[42] James, A.I. Eldridge, D.J. Moseby, K.E. (2010),“Foraging pits, litter and plant germination in an arid shrubland” J. Arid. Environ., 516.

[43] Eldridge, D.J. Koen, T.B. Killgore, A. Huang,N. Whitford, W.G. (2012), “Animal foraging as a mechanism for sediment movement and soil nutrient development: Evidence from the semi-arid Australian woodlands and the Chihuahuan Desert”,Geomorphology., 157-158, 131-41.

[44] Verdon, S.J. Gibb, H. Leonard, S.W.J. (2016),“Net effects of soil disturbance and herbivory on vegetation by a reestablished digging mammal assemblage in arid zone Australia”, J. Arid. Environ.,133, 29-36.

[45] Chapin, S.F. (1980), “The mineral nutrition of wild plants”, Annu. Rev. Ecol. Syst., 11, 233-60.

[46] Canals, R.M. and Sebastià, M.T. (2000), “Soil nutrient fluxes and vegetation changes on molehills”,J. Veg. Sci., 11, 23-30.

[47] Garkaklis, M.J. Bradley, J.S. Wooller, R.D. (1998),“The effects of woylie (Bettongia penicillata)foraging on soil water repellency and water infiltration in heavy textured soils in southwestern Australia”, Aust. J. Zool., 23, 492-496.

[48] Chapman, T.F. (2013), “Relic bilby (Macrotis lagotis) refuge burrows: assessment of potential contribution to a rangeland restoration program”, Rangeland. J.,35,167-80.

[49] Whitford,W.G.and Kay,F.R.(1999)“Biopedturbation by mammals in deserts: A review”,J. Arid. Environ., 41, 203-230.

[50] Noble, J.C. Muller, W.J. Detling, J.K. Pfitzner,G.H. (2007), “Landscape ecology of the burrowing bettong: warren distribution and patch dynamics in semiarid eastern Australia”, Austral. Ecol., 32, 326-337.

[51] Davidson, A.D. Detling, J.K., Brown, J.H., 2012.Ecological roles and conservation challenges of social, burrowing, herbivorous mammals in the world’s grasslands. Front Ecol Environ. 10, 477-486.

[52] Grinath, J.B. Deguines, N. Chesnut, J.W. Prugh,L.R. Brashares, J.S. Suding, K.N. (2018),“Animals alter precipitation legacies: Trophic and ecosystem engineering effects on plant community temporal dynamics”. J Ecol., 106(4), 1454-1469.

[53] Koontz, T.L. and Simpson, H.L. (2010), The composition of seed banks on kangaroo rat Dipodomys spectabilis mounds in a Chihuahuan Desert grassland”, J. Arid. Environ., 74, 1156-1161.

[54] Newell, J. (2008), “The role of the reintroduction of greater bilbies (Macrotis lagotis) and burrowing bettongs (Bettongia lesueur) in the ecological restoration of an arid ecosystem: foraging diggings,diet and soil seed banks”, PhD Thesis, University of Adelaide, Adelaide.

[55] Desmet, P.G. and Cowling, R.M. (1999), “Patch creation by fossorial rodents: a key process in the revegetation of phytotoxic arid soils”, J. Arid.Environ., 43, 35-45.

[56] Eldridge, D.J. Woodhouse, J.N. Curlevski, N.J.A.Hayward, M. Brown, M.V. Neilan, B.A. (2015),“Soil-foraging animals alter the composition and cooccurrence of microbial communities in a desert shrubland”, Isme. J., 9, 2671-2681.

[57] James, A.I. Eldridge, D.J. Hill, B.M. (2009),“Foraging animals create fertile patches in an Australian desert shrubland”, Ecography., 32, 723-732.

[58] Kitajima, K. and Tilman, D. (1996), “Seed banks and seedling establishment on an experimental productivity gradient”, Oikos., 76, 381-391.

[59] Canals, R.M. Herman, D.J. Firestone, M.K. (2003),“How disturbance by fossorial mammals alters N cycling in a California annual grassland”, Eco., 84,875-881.

[60] Newediuk, L.J. Waters, I. Hare, J.F. (2015), “Aspen parkland altered by Richardson’s ground squirrel (Urocitellus richardsonii Sabine) activity: the good,the bad, and the not so ugly?”, Can. Field,Nat., 129,331-341.

[61] Bancroft, W.J. Roberts, J.D. Garkaklis, M.J. (2005),“Burrowing sea birds drive decreased diversity and structural complexity, and increased productivity in insular-vegetation communities”,Aust. J. Bot., 53,231-241.

[62] Godó, L. Tóthmérész, B. Valkó, O. Tóth, K. Réka, K.Szilvia, R. Kelemen, A. Török, P.Švamberková, E.Balázs, D. (2018), “Ecosystem engineering by foxes is mediated by the landscape context-A case study from steppic burial mounds”, Ecol. Evol., 8.

[63] Whitford,W.G.and Kay,F.R.“Biopedturbation by mammals in deserts: A review”J. Arid. Environ., 41, 203-230.

[64] Kurek, P. Kapusta, P. Holeksa, J. (2014), “Burrowing by badgers (Meles meles) and foxes (Vulpes vulpes)changes soil conditions and vegetation in a European temperate forest”, Ecol. Res., 29, 1-11.

[65] Müller, J. Heinze, J. Joshi, J. (2014), “Influence of experimental soil disturbances on the diversity of plants in agricultural grasslands”, J. Plant. Ecol., 7,509-517.

[66] Foster. B. and Gross, K. (1998), “Species richness in a successional grassland: Effects of nitrogen enrichment and plant litter”, Ecol., 79, 2593-2602.

[67] Xiong, S. and Nilsson, C. (1999), “The effects of plant litter on vegetation: A meta-analysis”, J.Ecol.,87, 984-994.

[68] Paschke, M.W. McLendon, T. Redente, E.F. (2000),“Nitrogen availability and old-field succession in a shortgrass steppe”, Ecosystems., 3, 144-158.

[69] Janeček, Š. Janečková, P. Lepš, J. (2007), “Effect of competition and soil quality on root topology of the perennial grass Molinia caerulea”, Preslia., 79, 23-32.

[70] Deák, B. Tóthmérész, B. Valkó, O. SudnikWójcikowska, B. Moysiyenko, II. Bragina,T.M. (2016),“Cultural monuments and nature conservation: The role of kurgans in maintaining steppe vegetation”, Biodivers. Conserv., 25, 2473-2490.

[71] Eldridge, D.J. James, A.I. (2009), “Soil-disturbance by native animals plays a critical role in maintaining healthy Australian landscapes”, Ecol. Manag. Restor.,10, 27-34.

[72] James, A.I. Eldridge, D.J. Koen, T.B. Moseby,K.E. (2011), “Can the invasive European rabbit (Oryctolagus cuniculus) assume the soil engineering role of locally-extinct natives?”, Biol. Invasions.,13,3027-3038.

[73] Walde, A.D. Walde, A.M. Delaney, D.K. Pater, L.L.(2009), “Burrows of Desert Tortoises (Gopherus agassizii) as Thermal Refugia for Horned Larks (Eremophila alpestris) in the Mojave Desert”,Southwest. Nat., 54, 375-381.

[74] Sangha, K.K. Jalota, R.K. Midmore, D.J. (2006),“Litter production, decomposition and nutrient release in cleared and uncleared pasture systems of central Queensland”, Australia. J. Trop. Ecol., 22,177-189.

[75] Dirks, I. Navon, Y. Kanas, D. Dumbur, R.Grünzweig, José. (2010), “Atmospheric water vapor as driver of litter decomposition in Mediterranean shrubland and grassland during rainless seasons”,Glob.Chang. Biol., 16, 2799-2812.

[76] De Villiers, M.S. Van Aarde, R. (1994), “Aspects of habitat disturbance by Cape porcupines in a savanna ecosystem”, S. Afr. J. Zool., 29.

[77] De Schaetzen, F. Van Langevelde, F. Wallisdevries,M.F. (2018), “The influence of wild boar (Sus scrofa) on microhabitat quality for the endangered butterfly Pyrgus malvae in the Netherlands”, J.Insect.Conserv., 22, 51-59.

[78] Weiss, S.B. Murphy, D.D. White, R.R. (1988) “Sun,slope, and butterflies: topographic determinants of habitat quality for Euphydryas editha”, Ecol., 69,1486-1496.

[79] Roy, D.B. Thomas, J.A. (2003), “Seasonal variation in the niche, habitat availability and population fluctuations of a bivoltine thermophilous insect near its range margin”, Oecologia., 134,439-444.

[80] Streitberger, M. Rose, S. Gabriel, H. Fartmann, T.(2014), “The role of a mound-building ecosystem engineer for a grassland butterfly”, J. Insect.Conserv., 18, 745-751.

[81] Seifan, M. Tielbo¨rger, K. Schloz-Murer, D. Seifan,T. (2010), “Contribution of molehill disturbances to grassland community composition along a productivity gradient” Acta. Oecol., 36,569-577.

[82] Gro¨ning, J. Krause, S. Hochkirsch, A. (2007),“Habitat preferences of an endangered insect species,Cepero’s groundhopper (Tetrix ceperoi)”, Ecol. Res.,22, 767-773.

[83] Warren, S.D. Bu¨ttner, R. (2008), “Active military training areas as refugia for disturbance-dependent endangered insects”, J. Insect. Conserv., 12, 671-676.

[84] Tscho¨pe, O. Tielbo¨rger, K. (2010), “The role of successional stage and small-scale disturbance for establishment of pioneer grass Corynephorus canescens”, Appl. Veg. Sci., 13, 326-335.

[85] Fleischer, K. Streitberger, M. Fartmann, T. (2013),“The importance of disturbance for the conservation of a low-competitive herb in mesotrophic grasslands”, Biologia., 68, 398-403.

[86] Eldridge, D.J. Whitford, W.G. (2009), “Badger (Taxidea taxus) disturbances increase soil heterogeneity in a degraded shrubsteppe ecosystem”,J. Arid. Environ., 73, 66-73.

[87] Read, J.L. Carter, J. Moseby, K.M. Greenville, A.(2008), “Ecological roles of rabbit, bettong and bilby warrens in arid Australia”, J. Arid. Environ., 72,2124-2130.

[88] Friend, G.R. (1993), “Impact of fire on small vertebrates in mallee woodlands and heathlands of temperate Australia: a review”, Biol. Conserv., 65,99-114.

[89] Bao, F.Y. Wu, S.B. Su, C. Yang, Li. Zhang, F.H. Ma,G.Z. (2013), “Air temperature changes in a burrow of Chinese pangolin, Manis pentadactyla, in winter”,Folia. Zool., 62 (1), 42-47.

[90] Wu, S.B. Ma, G.Z. Chen, H. Xu, Z. Li, Y. Liu, N.(2004), “A preliminary study on burrow ecology of Manis pentadactyla”, The journal of applied ecology.,15, 401-7. [In Chinese].

[91] Sun, N.C.M. Sompud, J. Pei, K.J.C. (2018), “Nursing period, behavior development, and growth pattern of a newborn Formosan pangolin (Manis pentadactyla penta-dactyla) in the wild”, Trop.Conserv. Sci., 11,1-6.

[92] Lim, N.T.L. Ng, P. (2008), “Predation on Manis javanica by Python Reticulatus in Singapore”,Hamadryad., 32 (1), 62-65.

[93] Pike, D.A. and Mitchell, J.C. (2013), “Burrowdwelling ecosystem engineers provide thermal refugia throughout the landscape”, Anim. Conserv.,16(6), 694-703.

[94] Deutsch, C. Tewksbury, J. Huey, R. Sheldon, K.Ghalambor, C. Haak, D. Martin, P. (2008),“Impacts of climate warming on terrestrial ectotherms across latitude”, Proc. Natl. Acad. Sci.USA., 105, 6668-6672.

[95] Huey, R.B. Deutsch, C.A. Tewksbury, J.J. Vitt, L.J.Hertz, P.E. Alvarez Pérez H.J. Garland, T.Jr.(2009),“Why tropical forest lizards are vulnerable to climate warming”, Proc. R. Soc. Lond., 276,1939-1948.

[96] Sinervo, B. Méndez-de-la-Cruz, F. Miles, D.Heulin, B. Bastiaans, E. Cruz, M. Lara Resendiz,R. Martínez-Méndez, N. Calderon-Espinosa, M.Meza, R. Gadsden, H Avila, L.J. Morando, M. De la Riva,I. Victoriano, P. Rocha, C. Ibargüengoytía, N.Puntriano, C. Massot, M. Sites, J.J. (2010),“Erosion of Lizard Diversity by Climate Change and Altered Thermal Niches” Science., 328, 894-899.

[97] Hailey, A. Coulson, I.M. (1996), “Temperature and the tropical tortoise Kinixys spekii: constraints on activity level and body temperature”, J. Zool. Lond.,240, 523-536.

[98] Lagarde, F. Louzizi, T. Slimani, T. El Mouden, E.l.H.Ben Kaddour, K. Moulherat, S. Bonnet, X.2012),“Bushes protect tortoises from lethal overheating in arid areas of Morocco”, Environ. Conserv.,39, 172-182.

[99] Wright, J. Jones, C. (2006), “The Concept of Organisms as Ecosystem Engineers Ten Years On:Progress, Limitations, and Challenges”, BioSci., 56,203-209.

[100] Jefferies, R.L. (2000), “Allochthonous inputs:integrating population changes and food web dynamics”, Trends. Ecol. Evol., 15, 19-22.

[101] Markwell, T.J. Daugherty, C.H. (2002), “Invertebrate and lizard abundance is greater on seabirdinhabited islands than on seabird-free islands in the Marlborough Sounds, New Zealand”,Ecoscience., 9,293-299.

[102] Jackson, D.R. Milstrey, E.G. (1989), “The fauna of gopher tortoise burrows”, Pages 86-98 in Gopher tortoise relocation symposium proceedings (JE Diemer, DR Jackson, JL Landers, JN Layne,and DA Wood, editors). Florida Game and Fresh Water Fish Commission Nongame Wildlife Program, Technical Report., 5, 1-109.

[103] Hancox, M. (1988), “The nidiculous fauna of badger setts”, Entomologist’s monthly magazine.,124, 93-95.

[104] Galvez-Bravo, L. Belliure, J. Rebollo, S. (2008),“European rabbits as ecosystem engineers:Warrens increase lizard density and diversity”, Biodivers.Conserv., 18, 869-885.

[105] Kretzer, J.E. and Cully, J.F. (2001), “Effects of black-tailed prairie dogs on reptiles and amphibians in Kansas shortgrass prairie”, Southwest. Nat., 46,171-177.

[106] Reichman, O.J. and Seabloom, E.W. (2002), “The role of pocket gophers as subterranean ecosystem engineers”, Trends. Ecol Evol., 17, 44-50.

[107] Hawkins, L.K. Nicoletto, P.F. (1992), “Kangaroo rat burrows structure the spatial organization of ground dwelling animals in a semiarid grassland”, J. Arid.Environ., 2, 199-208.

[108] Di Blanco, Y.E. Desbiez, A.L.J. Di Francescantonio,D. Di Bitetti, M.S. (2020), “Excavations of giant armadillos alter environmental conditions and provide new resources for a range of animals”, J.Zool., 311.

[109] Luckenbach,R.A.(1982),“Ecology and management of the desert tortoise (Gopherus agassizii) in California”, Pages 1-38 in North American tortoises: conservation and ecology(R.B. Bury, editor). United States Fish and Wildlife Service, Washington, D.C. Wildlife Research Report., 12, 1-126.

[110] Lomolino, M.V. and Smith, G.A. (2004), “Terrestrial vertebrate communities at black-tailed prairie dog (Cynomys ludovicianus) towns”, Biol. Conserv.,115, 89-100.

[111] Challender, D. Wu, S. Kaspal, P. (2019), “Manis pentadactyla. The IUCN Red List of Threatened Species 2019: eT12764 A123585318”, Available from: http://dx.doi.org/ 10.2305/IUCN.UK.2019-3.RLTS.T12764A123585318.en.

[112] Shi, Y.Q. (1985), “Ant eating habits of pangolins”,Wild Animals., 28 (6), 11-13. [In Chinese].

[113] Fang, L.X. Wang, S. (1980), “A preliminary survey on the habits of pangolin”, Mem Beijing Nat Hist Museum., 7, 1-6. [In Chinese].

[114] Wu, S. Liu, N. Zhang, Y. Ma, G. (2004), “Assessment of threatened status of Chinese pangolin (Manis pentadactyla)”, Chinese J. Appl. Environ. Biol., 10 (4), 456-461. [In Chinese].

[115] Su, C. (2011), “Study on burrowburrow Habitat selection and temperature characteristics of Manis Pentadactyla [D]”, Guangdong: South China Normal University. [In Chinese].

[116] Heath, M.E. (1992), “Manis pentadactyla”, Mam.Sp., 414, 1-6.

[117] Wu, S. Ma, G. Chen, H. Xu, Z. Li, Y. Liu, N. (2004),“A preliminary study on burrow ecology of Manis pentadactyla. Chin”, J. Appl. Environ. Biol., 15 (3),401-407. [In Chinese].

[118] Wu, S.B. Ma, G.Z. Liao, Q.X. Lu, K.H. (2005),“Studies of Conservation Biology on Chinese Pangolin”, Chinese Forest Press, Beijing., [In Chinese].

[119] Fan, C.Y. (2005), “Burrow Habitat of Formosan Pangolins (Manis pentadactyla pentadactyla) at Feitsui Reservoir”, M.Sc. Thesis, National Taiwan University, Taipei, Taiwan. [In Chinese].

[120] Lin, J.S. (2011), “Home Range and Burrow Utilization in Formosan Pangolin (Manis pentadactyla pentadactyla) at Luanshan, Taitung”,M.Sc. Thesis, National Pingtung University of Science and Technology, Pingtung, Taiwan. [In Chinese].

[121] O'Mcilia, M.F. Knopf, F.L. Lewis, J.C. (1982),“Some conscquences of competition between prairie dogs and beef cattle”, J. Range. Man., 35, 580-585.

[122] Agnew, W. Uresk, D.W. Hansen, R.M. (1986), “Flora and fauna associated with prairie dog colonies and adjacent ungrazed mixed grass prairie in western South Dakota”, J. Range. Manage., 39:135-139.

[123] Knopf, F.L. (1994), “Avian assemblages on altered grasslands”, Stud. Avian. Biol., 15, 247-257.

[124] Miller., Brian. Ceballos. Gerardo. Reading. Richard.(1994), “The Prairie Dog and Biotic Diversity”,Conserv. Biol., 8, 677-681.

[125] Eldridge, D.J. Costantinides, C. Vine, A. (2006),“Short-Term Vegetation and Soil Responses to Mechanical Destruction of Rabbit (Oryctolagus cuniculus L.) Warrens in an Australian Box Woodland”, Restor. Ecol., 14, 50-59.

[126] Farron, S.J. Hughes, Z.J. FitzGerald, D.M. Strom,K.B. (2020), “The impacts of bioturbation by common marsh crabs on sediment erodibility: A laboratory flume investigation”, Estuar. Coast. Shelf.S., 238, 106710.

[127] El-Bana, M.I. (2009), “Effects of the abandonment of the burrowing mounds of fat sand rat (Psammomys obesus cretzschamar 1828) on vegetation and soil surface attributes along the coastal dunes of North Sinai, Egypt”, J. Arid. Environ., 73, 821-827.

[128] Baker, B.W. Augustine, D.J. Sedgwick, J.A. Lubow,B. (2013), “Ecosystem engineering varies spatially:A test of the vegetation modification paradigm for prairie dogs”, Ecography., 36, 230-239.

[129] Gurney, C.M. Prugh, L.R. Brashares, J.S. (2015),“Restoration of Native Plants Is Reduced by RodentCaused Soil Disturbance and Seed Removal”,Range. Ecol. Manag., 68.

[130] Alba-Lynn, C. Detling, J.K. (2008), “Interactive disturbance effects of two disparate ecosystem engineers in North American shortgrass steppe”,Oecologia., 157: 269-78.

[131] Eldridge, D.J. Simpson, R. (2002), “Rabbit (Oryctolagus cuniculus L.) impacts on vegetation and soils, and implications for management of wooded rangelands”, Basic. Appl. Ecol., 3, 19-29.

[132] Eldridge, D.J. Kwork, A.B.C. (2008), “Soil disturbance by animals at varying spatial scales in a semi-arid Australian woodland”, Rangeland. J., 30,327-337.

[133] Sanders, D. Van Veen, F.F.J. (2011), “Ecosystem engineering and predation: The multi-trophic impact of two ant species”, J. Anim. Ecol., 80, 569-76.

[134] Hinze, A. Pillay, N. Grab, S. (2006), “The burrow system of the African ice rat Otomys sloggetti robertsi”, Mamm. Biol., 71, 356-365.

[135] Gharajehdaghipour, D. Roth, J.D. Fafard, P.M.Markham, J.H. (2016), “Arctic foxes as ecosystem engineers: increased soil nutrients lead to increased plant productivity on fox dens”, Sci. Rep., 6,24020.

[136] Ayarbe, J.P. Kieft, T.L. (2000), “Mammal mounds stimulate microbial activity in a semiarid shrubland”,Ecol., 81(4), 1150-1154.

[137] Hall,K.and Lamont,N.(2003)“Zoogeomorphology in the Alpine: Some observations on abiotic-biotic interactions”,Geomorphology., 55, 219-234. 10.1016/S0169-555X(03)00141-7.

[138] Nummi, P. and Holopainen, S. (2014), “Wholecommunity facilitation by beaver: Ecosystem engineer increases waterbird diversity”, Aqua.Conserv., 24.

[139] Duval, B.D. and Whitford, W.G. (2012),“Reintroduced prairie dog colonies change arthropod communities and enhance burrowing owl foraging resources”, Immed. Sci. Ecol., 1, 12-23.

[140] Orwin, K.h. Wardle, D.A. Towns, D.R.S. John, M.G.Bellingham, P.J. Jones, C. Fitzgerald, B.M.Parrish,R.G. Lyver, P.O.B. (2016), “Burrowing seabird effects on invertebrate communities in soil and litter are dominated by ecosystem engineering rather than nutrient addition”, Oecologia., 180.

[141] Duval, B.D. (2009), “Camel Spider (Solifugae) Use of Prairie Dog Colonies”, West. N. Am. Nat.,69, 272-276.

[142] Wijnhoven, S. Thonon, I. Velde, G. Van der. Leuven,R.S.E.W. Zorn, M. Eijsackers, H. Smits,A.J.M.(2006), “The Impact of Bioturbation by Small Mammals on Heavy Metal Redistribution in an Embanked Floodplain of the River Rhine”, Water.Air. Soil. Pollut., 177, 183-210.

[143] Ransom, T.S. (2011), “Earthworms, as ecosystem engineers, influence multiple aspects of a salamander's ecology”, Oecologia., 165, 745-54.

[144] Munro, N.T. McIntyre, S. Macdonald, B.Cunningham, S.A. Gordon, I.J. Cunningham, R.B.Manning, A.D. (2019), “Returning a lost process by reintroducing a locally extinct digging marsupial”,PeerJ., 7. e6622.

[145] Ross, C.E. Munro, N.T. Barton, P.S. Evans,M.J. Gillen, J. Macdonald, B.C.T. McIntyre, S.Cunningham, S.A. Manning, A.D. (2019), “Effects of digging by a native and introduced ecosystem engineer on soil physical and chemical properties in temperate grassy woodland”, PeerJ., 7. e7506.

[146] Lindtner, P. Gajdoš, P. Stašiov, S. Čiliak, M. Pech,P. Kubovčík, V. (2019), “Spider (Araneae) and harvestman (Opiliones) communities are structured by the ecosystem engineering of burrowing mammals”, Insect. Conserv. Diver., 13.

[147] Wilby, A. Shachak, M. Boeken, B. (2001),“Integration of ecosystem engineering and trophic effects of herbivores”, Oikos., 92, 436-444.

[148] Grinath, J.B. Larios, L. Prugh, L.R. Brashares, J.S.Suding, K.N. (2019), “Environmental gradients determine the potential for ecosystem engineering effects”, Oikos., 128.

[149] Boeker, C. and Geist, J. (2016), “Lampreys as ecosystem engineers: burrows of Eudontomyzon sp. and their impact on physical, chemical, and microbial properties in freshwater substrates”,Hydrobiologia., 777.

[150] Dunham, A.E. (2011), “Soil disturbance by vertebrates alters seed predation, movement and germination in an African rain forest”, J. Trop. Ecol., 27, 581-589.

[151] Noble, J.C. (1993), “Relict Surface-Soil Features in Semi-Arid Mulga (Acacia Aneura) Woodlands”,Rangel. J., 15(1), 48-70.

[152] Hagenah, N. Bennett, N.C. Kitchener, A. (2013), “Mole rats act as ecosystem engineers within a biodiversity hotspot, the Cape Fynbos”, J. Zool., 289.

[153] Clark, K.L. Branch, L.C. Hierro, J.L. Villarreal, D.(2016), “Burrowing herbivores alter soil arbon and nitrogen dynamics in a semi-arid ecosystem,Argentina”, Soil. Biol. Biochem., 103, 253-261.

[154] Zhang, Y.M. Zhang, Z.B. Liu, J. (2003), “Burrowing rodents as ecosystem engineers: The ecology and management of plateau zokors Myospalax fontanierii in alpine meadow ecosystems on the Tibetan Plateau”, Mammal. Rev., 33, 284-294.

[155] Lynn, J.S. Canfield, S. Conover, R.R. Keene, J.Rudgers, J.A. (2018), “Pocket gopher (Thomomys talpoides) soil disturbance peaks at mid-elevation and is associated with air temperature, forb cover, and plant diversity”, Arct. Antarct. Alp. Res., 50, 1. e1487659.

[156] Davidson, A.D. and Lightfoot, D.C. (2008),“Burrowing rodents increasrl and scape heterogeneity in a desert grassland”, J. Arid.Environ., 72, 1133-1145.

[157] Martínez-Estévez, L. Balvanera, P. Pacheco, J.Ceballos, G. (2013), “Prairie Dog Decline Reduces the Supply of Ecosystem Services and Leads to Desertification of Semiarid Grasslands”, PloS. one.,8(10), e75229.

[158] Parsons, M.A. Barkley, T.C. Rachlow, J.L. JohnsonMaynard, J.L. Johnson, T.R. Milling, C.R.Hammel,J.E. Leslie, I. (2016), “Cumulative effects of an herbivorous ecosystem engineer in a heterogeneous landscape”, Ecosphere., 7. 10.1002/ecs2.1334.

[159] Newediuk, L.J. Hare, J.F. (2020), “Burrowing Richardson’s ground squirrels affect plant seedling assemblages via environmental but not seed bank changes”, Curr. Zool., 66(3), 219-226.

[160] Eldridge, D.J. (2011), “The resource coupling role of animal foraging pits in semi-arid woodlands”,Ecohydrology., 4, 623-630.

[161] McKechnie, S. (2006), “Biopedturbation by an island ecosystem engineer: Burrowing volumes and litter deposition by sooty shearwaters (Puffinus griseus)”, New. Zeal. J. Zool., 33(4), 259-265.

[162] Jouquet, P. Dauber, J. Lagerlöf., J. Lavelle, P. (2006),“Soil invertebrates as ecosystem engineers:Intended and accidental effects on soil and feedback loops”,Appl. Soil. Ecol., 32, 153-164.

[163] Clayton, J. Gardner, M. Fenner, A. Bull, M. (2019),“Co-occupancy of spider-engineered burrows within a grassland community changes temporally”,Austral. Ecol., 45.

[164] Bryce, R. van der Wal, R. Mitchell, R. Lambin, X.(2013), “Metapopulation Dynamics of a Burrowing Herbivore Drive Spatio-temporal Dynamics of Riparian Plant Communities”, Ecosystems.,16.

[165] Bancroft, W.J. Garkaklis, M.J. Roberts, J.D. (2005),“Burrow building in seabird colonies: a soil-forming process in island ecosystems”, Pedobiologia., 49,149-165.

Downloads

Issue

Vol. 3 , Iss. 3 (July 2021)

Article Type

Reviews

License

Copyright and Licensing

The authors shall retain the copyright of their work but allow the Publisher to publish, copy, distribute, and convey the work.

Journal of Zoological Research publishes accepted manuscripts under Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC 4.0). Authors who submit their papers for publication by Journal of Zoological Research agree to have the CC BY-NC 4.0 license applied to their work, and that anyone is allowed to reuse the article or part of it free of charge for non-commercial use. As long as you follow the license terms and original source is properly cited, anyone may copy, redistribute the material in any medium or format, remix, transform, and build upon the material.

License Policy for Reuse of Third-Party Materials

If a manuscript submitted to the journal contains the materials which are held in copyright by a third-party, authors are responsible for obtaining permissions from the copyright holder to reuse or republish any previously published figures, illustrations, charts, tables, photographs, and text excerpts, etc. When submitting a manuscript, official written proof of permission must be provided and clearly stated in the cover letter.
The editorial office of the journal has the right to reject/retract articles that reuse third-party materials without permission.

Journal Policies on Data Sharing

We encourage authors to share articles published in our journal to other data platforms, but only if it is noted that it has been published in this journal.