The Use of Intrinsic Markers for Studying the Migratory Movements of Bats

. 2021 Dec 6;11(12):3477. doi: 10.3390/ani11123477

Study Species	Common Name	Migratory Status	Intrinsic Marker	Region	Regression Method	Precipitation	Gender	Equation	n	r²	p-Value	Reference
Barbastella barbastellus	Western barbastelle	sedentary	δ²H	Europe	RMA	Mean annual precipitation	combined	δ²H_f = (1.37 × δ²H_p) − 5.52	217	0.67	<0.001	[15]
Barbastella barbastellus	Western barbastelle	sedentary	δ²H	Europe	LMM / REML	Mean annual precipitation	combined	δ²H_f = (1.07 × δ²H_map) − 16.84	178	0.72	NR*	[40]
Chaerephon cf. pumilus	Little free-tailed bat	sedentary	δ¹⁵N	Africa	OLS	N/A*	combined	¹⁵N_f = (−0.01 × elevation) + 28.78	55	0.32	<0.001	[61]
Eidolon helvum	Straw-colored fruit bat	migratory	δ²H	Africa	RMA	Mean annual precipitation	combined	δ²H_f = (1.52 × δ²H_p) − 54.09	193	NR*	<0.001	[30]
Epomophorus crypturus	Peters’s epauletted fruit bat	likely non-migratory	δ²H	Africa	RMA	Mean annual precipitation	combined	δ²H_f = (1.5 2 × δ²H_p) − 54.09	193	NR*	<0.001	[30]
Epomophorus wahlbergi	Wahlberg’s epauletted fruit bat	likely non-migratory	δ²H	Africa	RMA	Mean annual precipitation	combined	δ²H_f = (1.52 × δ²H_p) − 54.09	193	NR*	<0.001	[30]
Epomophorus wahlbergi	Wahlberg’s epauletted fruit bat	likely non-migratory	δ¹³C, δ¹⁵N	Africa	OLS	N/A*	combined	elevation = 4635 − (67 × ¹⁵N_f) + (112 × ¹³C_f)	66, 65	0.22	0.004, 0.002	[61]
Epomops franqueti	Franquet’s epauletted fruit bat	likely non-migratory	δ²H	Africa	RMA	Mean annual precipitation	combined	δ²H_f = (1.52 × δ²H_p) − 54.09	193	NR*	<0.001	[30]
Eptesicus isabellinus	Meridional serotine	sedentary	δ²H	Europe	RMA	Mean annual precipitation	combined	δ²H_f = (1.37 × δ²H_p) − 5.52	217	0.67	<0.001	[15]
Eptesicus isabellinus	Meridional serotine	sedentary	δ²H	Europe	LMM / REML	Mean annual precipitation	combined	δ²H_f = (1.07 × δ²H_map) − 16.84	178	0.72	NR*	[40]
Eptesicus serotinus	Serotine bat	sedentary	δ²H	Europe	RMA	Mean annual precipitation	combined	δ²H_f = (1.37 × δ²H_p) − 5.52	217	0.67	<0.001	[15]
Eptesicus serotinus	Serotine bat	sedentary	δ²H	Europe	LMM / REML	Mean annual precipitation	combined	δ²H_f = (1.07 × δ²H_map) − 16.84	178	0.72	NR*	[40]
Hipposideros caffer	Sundevall’s roundleaf bat	sedentary	δ¹⁵N	Africa	OLS	N/A*	combined	¹⁵N_f = (−0.01 × elevation) + 28.78	55	0.32	<0.001	[61]
Hypsignathus monstrosus	Hammer-headed bat	likely non-migratory	δ²H	Africa	RMA	Mean annual precipitation	combined	δ²H_f = (1.52 × δ²H_p) − 54.09	193	NR*	<0.001	[30]
Lasionycteris noctivagans	Silver-haired bat	migratory	δ²H	North America	geostatistical model	Mean growing season precipitation	combined	δ²H_f = (0.70 × δ²H_p) − 40.65	NR*	0.67	<0.001	[20]
Lasiurus borealis	Eastern red bat	migratory	δ²H	North America	GLM	Mean annual precipitation	male	δ²H_f = (−0.82 × δ²H_p) − 58.80	17	0.33	0.0482	[226]
							female	δ²H_f = (1.35 × δ²H_p) − 6.30	36	0.31	0.0003
							juvenile	δ²H_f = (0.67 × δ²H_p) − 23.97	28	0.16	0.0143
							combined	δ²H_f = (0.48 × δ²H_p) − 26.10	81	0.07	0.0201
Lasiurus borealis	Eastern red bat	migratory	δ²H	North America	RMA	Mean growing season precipitation	male	δ²H_f = (1.48 × δ²H_p) + 13.95	20	0.69	<0.001	[67]
							female	δ²H_f = (1.75 × δ²H_p) + 18.02	44	0.29	<0.001
							combined	δ²H_f = (1.67 × δ²H_p) + 16.84	64	0.37	<0.001
Lasiurus borealis	Eastern red bat	migratory	δ²H	North America	RMA	Mean annual precipitation	combined	δ²H_f = (1.00 × δ²H_p) + 8.17	64	0.41	<0.001	[31]
Lasiurus cinereus	Hoary bat	migratory	δ²H	North America	NR*	Mean growing season precipitation	combined	δ²H_f = (0.7884 × δ²H_p) − 24.81	104	0.60	<0.001	[28]
Lasiurus cinereus	Hoary bat	migratory	δ²H	North America	OLS	Mean growing season precipitation	combined	δ²H_f = (0.73 × δ²H_p) − 42.61	117	0.55	<0.001	[19]
Lasiurus cinereus	Hoary bat	migratory	δ²H	North America	RMA	Mean June/July/August precipitation	combined	δ²H_f = (0.874 × δ²H_p) − 41.8	117	0.49	<0.001	[31]
Lissonycteris angolensis	Angolan fruit bat	sedentary	δ²H	Africa	RMA	Mean annual precipitation	combined	δ²H_f = (1.52 × δ²H_p) − 54.09	193	NR*	<0.001	[30]
Lissonycteris angolensis	Angolan fruit bat	sedentary	δ¹³C, δ¹⁵N	Africa	OLS	N/A*	combined	elevation = 4635 − (67 × ¹⁵N_f) + (112 * ¹³C_f)	66, 65	0.22	0.004, 0.002	[61]
Miniopterus natalensis	Natal long-fingered bat	migratory	δ¹⁵N	Africa	OLS	N/A*	combined	¹⁵N_f = (−0.01 × elevation) + 28.78	55	0.32	<0.001	[61]
Miniopterus schreibersii	Schreiber’s bat	migratory	δ²H	Europe	LMM	growing season precipitation	combined	δ²H_f = (0.62 × δ²H_isoscape) − 14.66	NR*	NR*	NR*	[227]
Miniopterus schreibersii	Schreiber’s bat	migratory	δ²H	Europe	LMM	growing season precipitation	combined	δ²H_wing = (0.64 × δ²H_isoscape) − 14.64	NR*	NR*	NR*	[227]
Myotis lucifugus	Little brown myotis	migratory	δ²H	North America	GLM	Mean annual precipitation	male	δ²H_f = (0.49 × δ²H_p) − 30.90	12	0.19	0.1527	[226]
							female	δ²H_f = (0.33 × δ²H_p) − 40.41	54	0.06	0.0492
							juvenile	δ²H_f = (1.09 × δ²H_p) − 9.31	12	0.40	0.1291
							combined	δ²H_f = (0.52 × δ²H_p) − 30.82	78	0.17	0.0002
Myotis lucifugus	Little brown myotis	migratory	δ²H	North America	OLS	Mean growing season precipitation	combined	δ²H_f = (2.69 × δ²H_p) + 96.93	NR*	0.63	<0.001	[172]
Myotis septentrionalis	Northern myotis	migratory	δ²H	North America	GLM	Mean annual precipitation	male	δ²H_f = (0.79 × δ²H_p) − 4.73	10	0.53	0.0088	[226]
							female	δ²H_f = (1.25 × δ²H_p) + 18.48	16	0.71	0.0001
							juvenile	δ²H_f = (1.65 × δ²H_p) + 17.64	7	0.47	0.0258
							combined	δ²H_f = (0.98 × δ²H_p) + 5.48	33	0.54	<0.0001
Myotis sodalis	Indiana bat	migratory	δ²H	North America	GLM	Mean annual precipitation	male	δ²H_f = (0.90 × δ²H_p) − 0.59	12	0.46	0.0115	[226]
							female	δ²H_f = (0.71 × δ²H_p) − 8.17	39	0.35	0.0001
							juvenile	δ²H_f = (2.18 × δ²H_p) + 30.33	8	0.63	0.0046
							combined	δ²H_f = (0.83 × δ²H_p) − 2.97	59	0.49	0.0001
Neoromicia nana	Banana pipistrelle	sedentary	δ¹⁵N	Africa	OLS	N/A*	combined	¹⁵N_f = (−0.01 × elevation) + 28.78	55	0.32	<0.001	[61]
Nyctalus leisleri	Leisler’s bats	migratory	δ²H	Europe	RMA	Mean annual precipitation	combined	δ²H_f = (1.27 × δ²H_p) − 7.35	178	NR*	<0.001	[34]
Nyctalus noctula	Common noctule	migratory	δ²H	Europe	RMA	Mean annual precipitation	combined	δ²H_f = (1.37 × δ²H_p) − 5.52	217	0.67	<0.001	[15]
Nyctalus noctula	Common noctule	migratory	δ²H	Europe	RMA	Mean annual precipitation	combined	δ²H_f = (1.27 × δ²H_p) − 7.35	178	NR*	<0.001	[34]
Nyctalus noctula	Common noctule	migratory	δ²H	Europe	LMM	Mean annual precipitation	combined	δ²H_f = (0.92 × δ²H_p) − 30.72	335	NR*	NR*	[63]
Nycteris thebaica	Egyptian slit-faced bat	likely non-migratory	δ¹⁵N	Africa	OLS	N/A*	combined	¹⁵N_f = (−0.01 × elevation) + 28.78	55	0.32	<0.001	[61]
Perimyotis subflavus	Tri-colored bat	migratory	δ²H	North America	quadratic	Mean growing season precipitation	male	δ²H_f = (−0.036 × δ²H_p²)-(1.789 × δ²H_p) − 45.607	29	0.86	<0.01	[29]
Perimyotis subflavus	Tri-colored bat	migratory	δ²H	North America	quadratic	Mean growing season precipitation	female	δ²H_f = (−0.034 × δ²H_p²) − (1.606 × δ²H_p) − 40.375	27	0.75	<0.01	[29]
Pipistrellus cf. grandidieri	Dobson’s pipistrelle	sedentary	δ¹⁵N	Africa	OLS	N/A*	combined	¹⁵N_f = (−0.01 × elevation) + 28.78	55	0.32	<0.001	[61]
Pipistrellus pipistrellus	Common pipistrelles	sedentary?	δ²H	Europe	RMA	Mean annual precipitation	combined	δ²H_f = (1.27 × δ²H_p) − 7.35	178	NR*	<0.001	[34]
Pipistrellus nathusii	Nathusius’ pipistrelles	migratory	δ²H	Europe	RMA	Mean annual precipitation	combined	δ²H_f = (1.27 × δ²H_p) − 7.35	178	NR*	<0.001	[34]
Pipistrellus nathusii	Nathusius’ pipistrelles	migratory	δ²H	Europe	NR*	Mean annual precipitation	combined	δ²H_f = (0.74 × δ²H_p) − 83.96	458	NR*	NR*	[39]
Pipistrellus sp.		sedentary	δ¹⁵N	Africa	OLS	N/A*	combined	¹⁵N_f = (−0.01 × elevation) + 28.78	55	0.32	<0.001	[61]
Plecotus auritus	Brown long-eared bat	sedentary	δ²H	Europe	RMA	Mean annual precipitation	combined	δ²H_f = (1.37 × δ²H_p) − 5.52	217	0.67	<0.001	[15]
Plecotus auritus	Brown long-eared bat	sedentary	δ²H	Europe	LMM / REML	Mean annual precipitation	combined	δ²H_f = (1.07 × δ²H_map) − 16.84	178	0.72	NR*	[40]
Plecotus austriacus	Grey long-eared bat	sedentary	δ²H	Europe	RMA	Mean annual precipitation	combined	δ²H_f = (1.37 × δ²H_p) − 5.52	217	0.67	<0.001	[15]
Plecotus austriacus	Grey long-eared bat	sedentary	δ²H	Europe	LMM / REML	Mean annual precipitation	combined	δ²H_f = (1.07 × δ²H_map) − 16.84	178	0.72	NR*	[40]
Rhinolophus cf. clivosus	Geoffroy’s horseshoe bat	sedentary	δ¹⁵N	Africa	OLS	N/A*	combined	¹⁵N_f = (−0.01 × elevation) + 28.78	55	0.32	<0.001	[61]
Rhinolophus sp.		sedentary	δ¹⁵N	Africa	OLS	N/A*	combined	¹⁵N_f = (−0.01 × elevation) + 28.78	55	0.32	<0.001	[61]
Rousettus aegyptiacus	Egyptian fruit bat	sedentary	δ²H	Africa	RMA	Mean annual precipitation	combined	δ²H_f = (1.52 × δ²H_p) − 54.09	193	NR*	<0.001	[30]
Rousettus aegyptiacus	Egyptian fruit bat	sedentary	δ¹³C, δ¹⁵N	Africa	OLS	N/A*	combined	elevation = 4635 − (67 × ¹⁵N_f) + (112 × ¹³C_f)	66, 65	0.22	0.004, 0.002	[61]
Rousettus lanosus	Long-haired rousette	sedentary	δ¹³C, δ¹⁵N	Africa	OLS	N/A*	combined	elevation = 4635-(67 × ¹⁵N_f) + (112 × ¹³C_f)	66, 65	0.22	0.004, 0.002	[61]
Scotophilus dingani	African yellow bat	sedentary	δ¹⁵N	Africa	OLS	N/A*	combined	¹⁵N_f = (−0.01 × elevation) + 28.78	55	0.32	<0.001	[61]

“NR*” signifies information that was not reported in the literature source while “N/A*” signifies the information in that column is not applicable. Regression methods are abbreviated in the table as follows: Reduced Major Axis (RMA), Linear Mixed Effects Model fit by Reduced Maximum Likelihood (LMM/REML), Ordinary Least Squares (OLS), Generalized Linear Model (GLM), Linear Mixed Effects Model (LMM).