Climate change drives subterranean spiders to exctinction: the response of Troglohyphantes spiders to global warming Marco Isaia Department of Life Sciences and Systems Biology - University of Turin, Italy ‘Caves are warm in winter and cold in summer’ 3 JUN 2012 11:41 7 DEC 2012 11:12 Aristotle, Meteorologica - 340 bC AUGUST -14 JUNE MAY -12 -10 C) ° VARIABLE CONSTANT -8 Mean Annual - Temperature ( Temperature -6 NOVEMBER -4 DECEMBER JANUARY -2 | | | | | | | 0 10 15 20 25 30 40 Distance from entrance (m) Thermical annual variability decreases progressively at increasing distance from entrance Smithson 1991. Theor Appl Climatol 44: 65–73 Grotta di Bossea - 108 Pi/CN Mean temperature 22/06/2012 – 18/04/2013 Cave (2 km deep) Cave (entrance) Outside C) ° Temperature in caves reaches an impressive stability Mean daily temperature ( temperature daily Mean Piano et al. 2015. Sc Tot Env, 536: 1007-1018 14- R2: 0.955 12- C) 10- ° ( int T 8- temperature 6- Internal 4- 2- LMM.Estimated βfor Text ±se: 0.901±0.041, p<0.001 | | | | | | | 2 4 6 8 10 12 14 External mean annual temperature Text (°C) Temperatures recorded inside caves provide an ideal approximation of the mean annual temperature outside Categorie biospeleologiche Sket 2008. J Nat Hist 42(21-22): 1549-1563 Model species Troglohyphantes spp. • Moderate to high levels of troglobiomorphy • Restricted or point-like ranges of distribution and proved monophyly • Narrow microclimatic requirements • Genetically structured population • Reduced dispersal ability Model species Troglohyphantes spp. • Moderate to high levels of troglomorphism • Restricted or point-like ranges of distribution • Narrow microclimatic requirements • Genetically structured population • Reduced dispersal ability Troglobiomorphy lucifer T. vignai T. pedemontanus T. Isaia et al., 2011. Mon Museo Reg Sc Nat. XLVII: 1-325 Deeleman-Reinhold, 1978. Op. Acad. Sci. et Artium Slovenica: 1-219 Isaia & Pantini, 2010. Zootaxa 2690: 1–18 Model species Troglohyphantes spp. • Moderate to high levels of troglobiomorphy • Restricted or point-like ranges of distribution and proved monophyly • Narrow microclimatic requirements • Genetically structured population • Reduced dispersal ability Distribution of the Western Alpine species O Troglohyphantes lucifuga O Troglohyphantes lanai O Troglohyphantes nigraerosae O Troglohyphantes bornensis O Troglohyphantes lucifer O Troglohyphantes henroti O Troglohyphantes vignai O Troglohyphantes konradi O Troglohyphantes pedemontanus O Troglohyphantes pluto O Troglohyphantes iulianae O Troglohyphantes bolognai 30 km Isaia et al., 2011. Mon Museo Reg Sc Nat. XLVII: 1-325 Isaia & Pantini, 2010. Zootaxa 2690: 1–18 Isaia et al., 2016. Inv. Syst., in press LINYPHIIDAE Gen. Troglohyphantes T. bornensis T. iulianae T. konradi T. lanai n.sp. T. lucifuga T. nigraerosae T. pedemontanus T. pluto T. vignai Isaia et al., 2011. Mon Museo Reg Sc Nat. XLVII: 1-325 «Because of the lack of reliable calibration points (e.g., fossils, relevant geological or biogeographical events) for the lineage, we relied on informed priors of the substitution rates of the cox1, based on available information for spiders» CROATIA SLOVENIA CROATIA CORSICA ALPI MARITTIME ALPI LIGURI ALPI LIGURI DINARIDES ALPI MARITTIME CORSICA Model species Troglohyphantes spp. • Moderate to high levels of troglobiomorphy • Restricted or point-like ranges of distribution • Narrow microclimatic requirements • Genetically structured population • Reduced dispersal ability GLM-ber. Estimated βfor Dst^2 ±se -0.0044±0.0008, p<0.001 100 - 80 - occurrence of 60 - Troglohyphantes 40 - Troglohyphantes of Probability 20 - spiders preferably occur inside caves | | | | | 0 10 20 30 40 60 where the Distance from entrance (m) temperature is stable Temperature range estimation based on GIS interpolation Mammola & Isaia, 2016. Inv Biol., 135(1): 20-30 Model species Troglohyphantes spp. • Moderate to high levels of troglobiomorphy • Restricted or point-like ranges of distribution • Narrow microclimatic requirements • Genetically structured population • Reduced dispersal ability Lacking shared haplotypes between caves and showing very reduced dispersal ability Mammola et al., 2015. Peer J 3:e1384 Model species Troglohyphantes spp. • Moderate to high levels of troglobiomorphy • Restricted or point-like ranges of distribution • Narrow microclimatic requirements • Genetically structured population • Reduced dispersal ability Troglohyphantes spiders are good candidates as climatic bioindicators Study area Western Italian Alps 33 hypogean sites 33x2 temperature dataloggers 2 years monitoring Presence Absence Troglohyphantes spp. 18 presence vs 15 absence points Torino 10 km | | Hygrochron i-Button temperature dataloggers Buco dell'Aria Calda Borna d'la Glace Gheisa d'la Tana Borna del Servais B Borna Maggiore di Pugnetto Caverna delle Streghe Balma Fumarella Sotterranei di Vernante Testa di Napoleone di Sambughetto Grotta del Bandito Castel Delfino Tana dell'Orso di dell'Orso Tana Partigiano di Rossana Fessura di di Verrogne Fessura Caverna dell'Om dell'Om Salvey Caverna Grotta di di Grotta Bergovei Barun Litrun The probability of Troglohyphantes occurrence decreases with increasing mean annual temperature GLM-ber. Estimated βfor Tint ±se: -0.543±0.249, p=0.02 1,0- occurrence 0,8- 0,6- Troglohyphantes of 0,4- 0,2- probability 0,0- Predicted | | | | | | | 2 4 6 8 10 12 14 Cave temperature (Tint ) (°C) Extending the trend to the regional scale: Ecological Niche Modeling 361 hypogean sites Presence Presence/absence data derived from Absence Isaia et al., 2011 Minimization of spatial correlation (Newbold., 2010) 5 out of 19 bioclimatic variables + Ice cover during LGM Modeling Torino Generalized linear models (GLM) Boosted Regression Trees (BRT) Maximum Entropy Model (MaxEnt) Projections - Present - LGM - High and low emission scenarios for 2050 and 2070 10 km | | PRESENT LGM (22,000 YEARS AGO) MaxEnt Mean AUC±sd = 0.873±0.09 BIOCLIMATIC SUITABILITY LOW Mean TSS±sd = 0.51±0.08 HIGH ICE EXTENT DURING Last Glacial Maximum Current climate projections overlay the known distribution of Troglohyphantes. Pleistocene: Southern border of the Alps very suitable Areas bordering the glacial masses acted as microrefugia during LGM Mammola Goodacre and Isaia, 2016. Ecography (in press) 2050 2070 -56% -58% LOW EMISSIONS LOW -62% -73% HIGH EMISSIONS BIOCLIMATIC SUITABILITY LOW HIGH A future general decline of suitability all over the range of distribution Mammola Goodacre and Isaia, 2016. Ecography (in press) HIGH --------------- PRESENT WORST CASE SCENARIO 2070 SCENARIO CASE WORST SUITABILITY BIOCLIMATIC ------------------ Presence LOW Approximately half of the current localities are predicted to be unsuitable Mammola Goodacre and Isaia, 2016. Ecography (in press) Temperature increase due to global warming poses serious concerns about the long-term survival of Troglohyphantes spiders 1,0- occurrence 0,8- . spp 0,6- 0,4- roglohyphantes T of 0,2- Probability 0,0- | | | | | | | 2 4 6 8 10 12 14 Mean annual cave temperature (Tint ) (°C) Mammola Goodacre and Isaia, 2016. Ecography (in press) Acknowledgements Elena Piano (jr) Marco Isaia (Help with field work) (Myself) Elenia Lazzaro (Help with field work) Giovanni Badino (Supervision - Physics) Stefano Mammola John Dejanaz (Co-author) (Help with field work) Francesco Tomasinelli (Photo credits) Miquel Arnedo (Genetic analysis) Paolo Pantini (Spider systematics) Sara Goodacre (Co-author) This reasearch was funded by Compagnia di San Paolo and Università di Torino Progetti di Ricerca di Ateneo 2011 and 2016 in the frame of FromCAVELAB microclimate to global change: caves as laboratories for the study of the effects of temperature on ecosystems and biodiversity and CAVEAT The dark side of climate change Photo credits Francesco Tomasinelli and Mauro Paschetta .