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Knowledge gaps and canopy openings: the importance of
Neotropical squirrels
John L. Koprowski University of Arizona
Knowledge gaps & canopy openings: the importance of Neotropical squirrels
John L. Koprowski, Professor of Wildlife Conservation
North American Red Squirrel Tamiasciurus hudsonicus
Red-tailed Squirrel Sciurus granatensis
I am grateful…
Especially:
Mauro Galetti Calebe Mendes
Ricardo Bovendorp
Marlon Zortéa
21 Sept - 11h30 CBMz
Dedicated to Richard “Thor” Thorington, Jr.
Because they’re cool!
“Ready for the Plenary talk”
+ =
A red squirrel is not a red squirrel is not a red squirrel…
27 misidentifications of South American red squirrels as a temperate zone species in disease literature
Today’s Road Map Why squirrels?
Patterns of diversity
Biased perception of squirrels
Knowledge gaps &
delineating our needs
What we have learned
Opportunities that await
– Response to disturbance
– Climate change
Koprowski
Conservation
Research
Laboratory
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PC 1
PC
2
MGRS
Abert's
Endangered
Species
Seeking science-based
solutions
SNRE
BiologicaI
Invasions
Forest Range & Climate
Human Dimensions
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500
600
1986 1990 1994 1998 2002 2006 2010
Year
Po
pu
lati
on
Siz
e
1999 2010
The people who are doing the hard work…
Squirrels as indicators
Mexico
Japan
Peru
China
South Africa
USA
A few current squirrel projects
Where have all the little trees
gone?
?
PhD ?
Mt. Graham red squirrel captive
breeding & artificial middens
Determinants of occupancy
of Big Cypress fox squirrels Kira Hefty
PhD USA
Marina Morandini
PhD Italy
Stuart Wells
PhD USA
Max Mazzella
MS USA Wildland fire as a
management tool
Squirrels…Why Squirrels?
Squirrels as models • Widespread
• Conspicuous
– Most are diurnal
– Medium-body size
– Large nests/burrows
– Obvious feeding sign
– Cameras/Hair tubes
• Indicators of
habitat
Models
• Indicator species
• Umbrella species
• Keystone species
• Medical models
• Forest regeneration
• Forest health
• Urban synanthrope
Koprowski J, Goldstein-Murphy E, Bennett K, Mendes C. 2016. Family Sciuridae (in D Wilson D, T Lacher Jr, R Mittermeier, Handbook of mammals of the World), Lynx Edicions.
African tree squirrels
Marmots
Holarctic ground squirrels
African ground squirrels
Southern Asian tree
squirrels
Holarctic tree squirrels
Flying squirrels
South American pygmy
squirrels
Giant tree squirrels
Other rodents
Relationships of squirrels
after Steppan et al. 2004
293 species
36 million years old and counting…
Jefferson’s squirrel, Douglassciurus jeffersoni
What really makes a squirrel a squirrel?
“Sciuromorph”
“Hystricomorph”
“Myomorph”
Remarkably conserved morphology
Diastema Incisors
Cheek teeth
Squirrels come in all shapes and sizes
3 kg 15 g
9 kg
Sciurillinae (1 sp): South American Pygmy Squirrel
Ratufinae (4 sp): Giant Tree Squirrels
Callosciurinae (37 sp): SE Asian Beautiful Squirrels
Xerinae (131 sp) Ground & African Squirrels
Sciurini (37 sp): American & N Eurasian Tree Squirrels
Pteromyini (52 sp) Flying Squirrels
More species in the tropics
181 arboreal species
Reversed cline in knowledge
A dearth of knowledge at global scale...
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Number of Publications
Pro
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rti
on
of
Sp
ecie
s
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Publications
Pro
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rtio
n Flying
Tree
An attempt…
Koprowski J, Goldstein-Murphy E, Bennett K, Mendes C. 2016. Family Sciuridae (in D Wilson D, T Lacher Jr, R Mittermeier, Handbook of mammals of the World), Lynx Edicions.
And a lack of knowledge has consequences…
World South America
IUCN categories of threat
66%
33%
0% 0% Data Deficient
Low Concern
Near Threatened
Vulnerable-Endangered-CriticallyEndangered
South America
What we know about the Sciuridae
are biased by a few northerly species
• Squirrels cache foods… Variable in tropics
• Squirrels can remove 100% of tree seeds
• Squirrels show early response to climate change
• Squirrels rarely are tied to zoonoses… Recent data from the Neotropics suggest important role
• Squirrel responses to fragmentation are
predictable and lead to increased
interaction rates
How many species do we have?
1961
Treatments of the South American Sciuridae
1993 2005 2012 2016
= 15 species
1915 2015 1997
25 species 13 species 11 species 19 species
We don’t even know how many
species we have!
21 Sept - 11h30 CBMz 39 – Mapa do atual conhecimento sobre a ecologia esquilos neotropicals – Calebe Mendes e Mauro Galleti
“These taxonomic hypotheses differ from previous treatments of South American squirrels … and they are ripe for testing by phylogenetic and phylogeographic analyses employing molecular data and methods.” - Mario de Vivo and Ana Paula Carmignotto Mammals of South America (Vol 2): 3
Basic ecological information is lacking
Partitioning of Igapo forests of Peruvian Amazon
Sciurillus pusillus
Sciurus igniventris
How do squirrels use the forest?
How do squirrels partition space?
Do squirrels exhibit
temporal partitioning?
Basic population data are lacking
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Sciurus granatensis seem similar to temperate squirrels
L M H
MV
P
Ecological roles & ecosystem services are poorly known
Ecosystem services provided
• Seed dispersal
• Seed preparation/planting
• Fungal dispersal
• Soil inoculation
• Pollination
• Food and pelt for consumptive use
Valuing Ecosystem Services
Human well
being
Indirect Drivers of Change Demographic Economic
Science & Tech Sociopolitical Cultural & Religious
Indirect Drivers of Change Demographic Economic
Science & Tech Sociopolitical Cultural & Religious
Direct Drivers of Change Climate
Nutrient loading Land use
Species introduction Overexploitation
Biodiversity
Ecosystem Function Ecosystem Goods and Services
Ecosystem services provided
by squirrels
Supporting Services Primary production
Provision of habitat
Nutrient cycling
Soil formation and retention
Production of atmospheric oxygen
Water cycling
Provisioning Services Food, fiber, and fuel
Genetic resources
Biochemicals
Fresh water
Regulating Services Invasion resistance
Herbivory
Pollination
Seed dispersal
Climate regulation
Pest regulation
Disease regulation
Natural hazard protection
Erosion regulation
Water purification
Cultural Services Spiritual and religious values
Knowledge system
Education and inspiration
Recreation and aesthetic values
Importance in seed dispersal
Attalea oleifera
Pimentel and Tabarelli 2004
Pollination of Flame of the Forest Butea monosperma
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Crow Tree Pie Sunbird Parakeet Bulbul Babbler White
Eye
Squirrel Bee
Pollinator
Ac
tiv
ity
Un
its
Visits/d
Handling TimePollen Grains
Fruit Set
Tandon et al. 2003
Fungi-
Squirrel
Cycle Fungi get
carbohydrates
Trees get nutrients
& moisture
Squirrels feed
on fungi Fungi grow
and produce
sporocarps
Feces with
spores, N-
fixing bacteria,
yeast Spores
germinate
Dispersal of Fungal Spores
0
10
20
30
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Feces Sporocarp Control
Source of Spores
Su
ccess (
%)
Kotter and Farentinos 1984
Sciurus aberti
Mycophagy is common…
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Sciur
us vulga
ris
Glauc
omys
sab
rinus
Tam
iasc
iuru
s hu
dsonicu
s
Tam
iasc
iuru
s do
uglasii
Sciur
us gris
eus
Sciur
us abe
rti
Sciur
us ariz
onen
sis
Sciur
us nay
arite
nsis
Sciur
us car
olinen
sis
Sciur
us niger
Glauc
omys
volan
s
Sciur
us lis
Squirrel Species
Fu
ng
i in
Die
t (%
)
Impacts of habitat loss, degradation and forest fragmentation
70% of forest in the world is <1 km from an edge
62% in the USA is < 150 m from an edge
This is the challenge….
y = -0.68x + 3.88
R 2
= 0.898 Eastern Gray Squirrel
y = -0.83x + 2.97
R 2
= 0.914 Fox Squirrel
y = -0.26x + 0.65
R 2
= 0.0474 Eurasian Red Squirrel
y = -0.43x + 0.90
R 2
= 0.286 Red Squirrel -6
-4
-2
0
2
4
6
0 2 4 6 8
ln Forest Size (ha)
ln D
en
sit
y (
sq
uir
rels
/ha)
Fragmentation and increased density…
100 ha
10/ha
1/ha
0.1/ha
Koprowski 2005
…and decreases home range size
5 Species of Sciurus:
12 S.vulgaris, 8 S. niger, 9 S. carolinensis, 2 S. griseus, 3 S. aberti
Males
y = 0.56x - 0.94
R2 = 0.542
Females
y = 0.45x - 0.92
R2 = 0.532
-2
0
2
4
6
0 2 4 6 8
ln Forest Area (ha)
ln H
om
e R
an
ge S
ize (
ha)
100 ha
5 ha
50 ha
Mt. Graham red
squirrel ecology
is focused around
a midden
Cover
Energy
Microclimate
Structure
Larderhoard
Traditional Sites
Near Territory Center
Gaps, edges, traffic & noise
High traffic
(50-100 cars/ day)
Medium traffic
(20- 40 cars/day)
Low traffic
(~10 cars/day)
Hsiang Ling Chen
Road Random line
Pro
ba
bilit
y o
f c
ros
sin
g
0.0
0.2
0.4
0.6
0.8
Observed
Predicted
37%
70%
47%
56%
Model: Linear group + distance to midden + season × sex + body mass
Distance to roads had little effect
Distance from roads (m)
0 100 200 300 400
Pro
ba
bil
ity o
f o
cc
urr
en
ce
0.0
0.2
0.4
0.6
0.8
1.0
Canopy closure was influential
Model: Max. canopy cover + season + distance to midden + slope
Maximum canopy cover (%)
0 20 40 60 80 100 120
Pre
dic
ted
rate
of
cro
ssin
g (
log
)
-10
-8
-6
-4
-2
0
2
4
6
Mapping a Landscape of Noise
Standardized traffic-noise stimulus- Controlled vehicle operation
Sampling grid (50 x 50 m)
Noise measurement (Average & Max)
Ordinary Kriging geostatistical interpolation
Noise mapping (Average & Max)
Indicators of bioimpacts of noise
Max Average
30 dB 75 dB
Traffic noise affected animal occurrence
Occupancy rate changes by 6% as traffic noise increases by 1 dB
occupancy < 50% when traffic noise level is > 40 dB
Equivalent continuous sound level (dB)
25 30 35 40 45 50 55
Pro
bab
ilit
y o
f o
ccu
rren
ce
0.0
0.2
0.4
0.6
0.8
1.0
30 dB difference = 8 times loudness
Natal Habitat Preference Induction - NHPI Mabry & Stamps 2008
Natal habitat Novel terrain
Who disperses?
Open Field
MIS
R2 = 0.23
p = 0.033
PhD Melissa Merrick
Settled sites are more like natal sites
Canopy Cover
Basal Area
Tree Height
Stem Density
Defoliation (-)
Individual natal area Individual settlement area
0 Mean difference
Individual pairwise comparisons tell us
that natal and settlement sites do not
differ
Responses to climate change
Food = seeds from
conifer cones
Cool/moist midden = closed cones
=
www.scarysquirrel.org
Do midden microclimates respond to
climate change?
External
Internal
Cones open less with constant cool
Cones
open
Surface
Cached
Predicted temperature increases could
change cache sites
% Opening = -6.56 + 0.640 Max Temp
Max cone opening
10 5 15 20
5
0
25
10
15
20
35 30
% C
on
e o
pen
ing
Maximum Temp (oC)
Present
Upward shifting of habitats
1oC 3oC 5oC
Desert
Montane
Forest
Sciurus arizonensis
Montane mammal
isolates
Sylvilagus nuttallii Tamiasciurus hudsonicus Microtus longicaudus
Sorex monticolus
Most mammals are in habitats that will persist
Nearly 20% have a high risk of
extinction
123 Mammals
in Arizona
18.3%
76.3% Less immediate impact –
Maintain current
management strategies
High risk of extinction –
Novel management
actions needed – 4
species of squirrel
Unknown risk of extinction –
Further study needed
Squirrels represent a vastly
underused scientific resource
What needs to be done? 1. A molecular assessment of squirrel
phylogeny
2. Incorporate into surveys and databases
3. Understanding the ecological role in the tropics:
a.) Agent of dispersal
b.) Response to disturbance and fragmentation
c.) Response to defaunation
d.) Consequences of the loss of squirrels
2015
2012
2009
2006
2003 1994
2000
Welcome
to ICAS 8!
2018
8th International Colloquium on Squirrels @squirrels2018 and on Facebook
National University of Ireland – Galway 4-8 June 2018
?
Obrigado
Contact info: John L. Koprowski, Professor Wildlife Conservation & Mgmt School of Natural Resources & the Environment University of Arizona Tucson, Arizona 85721 USA [email protected] @squirreldoc www.ag.arizona.edu/research/redsquirrel UniversityofArizonaConservationResearchLaboratory
