Biol. Rev. (2019), 94, pp. 1294–1316.

1294
doi: 10.1111/brv.12503

A review of Gloger’s rule, an ecogeographical

rule of colour: definitions, interpretations
and evidence
Kaspar Delhey∗
School of Biological Sciences, Monash University, 25 Rainforest Walk, 3800 Clayton, Victoria, Australia

ABSTRACT

Gloger’s rule is an ecogeographical rule that links animal colouration with climatic variation. This rule is named
after C.W.L. Gloger who was one of the first to summarise the associations between climatic variation and animal
colouration, noting in particular that birds and mammals seemed more pigmented in tropical regions. The term
‘Gloger’s rule’ was coined by B. Rensch in 1929 and included different patterns of variation from those described
by Gloger. Rensch defined the rule in two ways: a simple version stating that endothermic animals are predicted to
be darker in warmer and humid areas due to the increased deposition of melanin pigments; and a complex version
that includes the differential effects of humidity and temperature on both main types of melanin pigments – eu- and
phaeo-melanin. The blackish eu-melanins are predicted to increase with humidity, and decrease only at extreme low
temperatures, while the brown-yellowish phaeomelanins prevail in dry and warm regions and decrease rapidly with
lower temperatures. A survey of the literature indicates that there is considerable variation/confusion in the way Gloger’s
rule is understood (based on 271 studies that define the rule). Whereas the complex version is hardly mentioned, only
a quarter of the definitions are consistent with the simple version of Gloger’s rule (darker where warm and wet), and
most definitions mention only the effects of humidity (darker where wet). A smaller subset of studies define the rule
based on other correlated climatic and environmental variables such as vegetation, latitude, altitude, solar radiation,
etc., and a few even contradict the original definition (darker where cold). Based on the literature survey, I synthesised
the qualitative (N = 124 studies) and quantitative (meta-analytically, N = 38 studies, 241 effects) evidence testing the
simple version of Gloger’s rule (I found no tests of the complex version). Both lines of evidence supported the predicted
effects of humidity (and closely linked variables) on colour variation, but not the effects of temperature. Moreover,
humidity effects are not restricted to birds and mammals, as the data indicate that these effects also apply to insects.
This suggests that the simple version of Gloger’s rule as originally defined may not be valid, and possibly that the rule
should be re-formulated in terms of humidity effects only. I suggest, however, that more data are needed before such a
reformulation, due to potential publication biases. In conclusion, I recommend that authors cite Rensch when referring
to Gloger’s rule and that they make clear which version they are referring to. Future research should concentrate
on rigorously testing the validity and generality of both versions of Gloger’s rule and establishing the mechanism(s)
responsible for the patterns it describes. Since humidity seems to be the core climatic variable behind Gloger’s rule, I
suggest that the two most plausible mechanisms are camouflage and protection against parasites/pathogens, the latter
possibly through pleiotropic effects on the immune system. Understanding the processes that lead to climatic effects on
animal colouration may provide insights into past and future patterns of adaptation to climatic change.

Key words: pigmentation, melanin, climate, temperature, humidity, biogeography, Gloger’s rule, thermal melanism.

CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1295
II. A brief history of gloger’s rule . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1295
III. How is gloger’s rule defined in the literature? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1297

* Address for correspondence (Tel.: +61 409 149 668; E-mail: kaspar.delhey@monash.edu)

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A review of Gloger’s rule 1295

IV. Support for gloger’s rule . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1300

(1) Qualitative tests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1300
(2) Quantitative tests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1300
(a) Meta-analytical methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1300
(b) Meta-analytical results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1304
V. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1304
VI. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1310
VII. Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1310
VIII. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1310
IX. Supporting Information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1316

I. INTRODUCTION regions (Zink & Remsen, 1986; Caro, 2005; Delhey,

Ecology has few rules. Among those are ecogeographical
rules, which describe variation in form and function across
space and along climatic gradients, such as latitudinal
gradients in body size (Bergmann’s rule) or appendage size
(Allen’s rule). These rules were mostly coined early in the
20th century (Rensch, 1936; Mayr, 1942; although often
their roots are older) but interest in them has increased
recently. This renewed attention comes from the fact that
understanding spatial patterns driven by variation in climatic
parameters such as temperature or rainfall can help identify
and possibly predict ways in which organisms may respond
to future climatic change (Millien et al., 2006; Yom-Tov &
Geffen, 2011; Scheffers et al., 2016).
Associated with this current focus has come a push to
clearly define these rules and establish strong ways to test for
their validity. Such scrutiny has mainly concentrated on the
most-studied ecogeographical rule, Bergmann’s rule, leading
to robust discussion on what is and what is not covered by the
rule (Watt, Mitchell & Salewski, 2010; Olalla-Tárraga, 2011;
Watt & Salewski, 2011; Salewski & Watt, 2017). In addition,
comprehensive tests have revealed further uncertainties in
terms of the broad applicability and generality of Bergmann’s
rule (Riemer, Guralnick, & White, 2018). This level of
attention and thorough testing has yet to be applied to other
ecogeographical rules (but see Symonds & Tattersall, 2010).
One of the most enigmatic ecogeographical rules is
Gloger’s rule, which deals with patterns of spatial variation in
animal colour, mainly in birds and mammals (Delhey, 2017).
Animal colouration is one of the most complex aspects of
phenotypic variation, and fulfils a variety of key functions
including camouflage, signalling, protection against parasites
or abrasion, and thermoregulation, to name a few of the most
salient ones (Cuthill et al., 2017). Disruption of these patterns
of adaptation due to habitat degradation or future climate
change could have strong negative fitness effects (Roulin,
2014; Delhey & Peters, 2017). Hence, consistent patterns of
geographical variation in colouration associated with clear
climatic or spatial gradients may provide rare insights into
important selective drivers leading to animal colour variation.
Unfortunately, the kinds of patterns of variation that are
associated with Gloger’s rule are not always clear.
Gloger’s rule is commonly described as predicting that
animals should be darker coloured in warm and humid
2018). However, some definitions mention only humidity
or temperature, or refer to other correlated variables such
as latitude, solar radiation, vegetation structure, etc. and
combinations thereof (see Section III for details). This
multiplicity of interpretations means that determining the
generality and applicability of Gloger’s rule becomes very
difficult. Indeed, while some researchers claim that Gloger’s
rule applies broadly and has much stronger support than
Bergmann’s rule (Zink & Remsen, 1986), others dismiss
Gloger’s rule as a pattern lacking large-scale geographic
applicability (Lomolino, Riddle & Brown, 2006). This
confusion is exacerbated by the fact that the proposed
mechanisms leading to the patterns described by Gloger’s
rule are varied, including camouflage, protection against
parasites, protection against solar radiation, or pleiotropic
effects, to name the most popular ones (Delhey, 2017).
Clearly, a review of Gloger’s rule is needed to establish a
clear definition and assess the level of existing support.
In this review I aim to: (i) provide a brief account of
the historical context around Gloger’s rule and its original
definition; (ii) survey the literature to establish how Gloger’s
rule is used and compare it to the original definition; (iii)
assess the degree of published support for Gloger’s rule in its
different interpretations, summarising both qualitative and
quantitative tests (the latter by means of a meta-analysis);
and (iv) in light of these results discuss which mechanisms are
the most likely drivers of the patterns of variation described
by Gloger’s rule.
II. A BRIEF HISTORY OF GLOGER’S RULE
In 1833, Constantin Wilhelm Lambert Gloger published a
book (Gloger, 1833) detailing how the colouration of birds
and mammals varied with climate. He mainly referred to
European birds and mammals, drawing conclusions from
comparative work on museum specimens, leaning also
heavily on the contributions of predecessors such as Pallas
(Haffer, 1992; Glaubrecht & Haffer, 2010). Gloger’s main
motivation was taxonomic; he was concerned that many
putative species of birds were not valid taxonomic entities,
and rather represented varieties that differed in colouration
(and other traits) simply due to the effects of climate. Gloger

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1296
stressed that differences in colouration seem to be a plastic
response of the individual to the climate; under similar
environmental conditions individuals should converge in
colouration. His main conclusion was that pigmentation
(and colours in general) should become more intense at
lower latitudes, in warmer regions, with the main outcome
being that in general tropical birds should be not only
darker coloured, but also more showy and contrasting. He
also recognised that desert birds are in general paler even
though they inhabit warm areas, thus also acknowledging
the potential effects of humidity.
Apparently independently to Gloger’s work, Joel Asaph
Allen (Allen, 1877) published a brief paper summarising
several biogeographic patterns of phenotypic variation of
animals. This paper synthesised his knowledge on patterns of
geographic variation in North American birds and mammals,
based on his extensive field trips and work at museum
collections (Allen, 1871, 1874). Allen described patterns
of geographic variation in overall size (consistent with
Bergmann’s rule), appendage size [which would become
Allen’s rule (Rensch, 1929)] and colouration. The latter
referred to the fact that birds and mammals living in
wetter areas were darker than their counterparts in drier
regions, and similarly, that southern forms seemed to be
more pigmented than northern ones. Unlike Gloger, Allen
concluded that the effects of humidity or rainfall on animal
colouration were more important than those of temperature
or solar radiation. Similar to Gloger however, Allen also
thought that variation in colouration due to climate was
mainly a plastic response, and that there were no real
adaptive benefits to this variation. Nevertheless, he also
mentioned that in some cases colour variation may be useful
for camouflage, as it tends to match the colouration of
prevailing backgrounds.
In 1923, Karl Görnitz (Görnitz, 1923) assessed these
patterns of variation in greater detail, linking different
types of colours with their different pigmentary mechanisms
(mainly different types of melanin and carotenoids) as known
at that time. He largely agreed with the results from Gloger,
but clearly indicated that patterns of climatic variation
seemed to be due to the differential responses of both main
types of melanin found in animals: eu- and phaeo-melanin
(Solano, 2014). Chiefly, melanin deposition increases with
high temperature and decreases with low temperature,
whereby phaeo-melanin decreases first, while eu-melanin
only decreases with extreme cold. Dryness leads to a
decrease in eu-melanin and an increase in phaeo-melanin
(Görnitz, 1923).
Based on Gloger’s, Allen’s and Görnitz’ conclusions,
Bernhard Rensch (Rensch, 1929) proposed that the
consistent patterns of climate-linked geographic colour
variation should be called Gloger’s rule. While Rensch
recognised the contribution of Allen and Görnitz [and also
of others such as Kleinschmidt (Rensch, 1929)] he decided
to name the rule to honour Gloger due to priority. Thus, the
first time Gloger’s rule is mentioned as such (‘Glogersche Regel’)
is found in Rensch (1929) and this should be considered
Biological Reviews 94 (2019) 1294–1316 © 2019 Cambridge Philosophical Society
Kaspar Delhey
the original form of the rule. Gloger’s rule as formulated by
Rensch (1929, p. 160) is (original German version):
Die Glogersche Regel. Die Melanine der Warmblüter (vielleicht aller
Tiere) erfahren eine Steigerung durch Zunahme der Temperatur und
der Luftfeuchtigkeit. Starke Anreicherung von Melanin führt in den
Vogelfedern zur Ausbildung von Schillerstruktur (Interferenzfarben).
Trockenes heisses Klima steigert nur die Phaeomelanine
(gelbe ‘‘wüstenfarbige’’ Oxydationsstufen), während die Eumelanine
schwinden. Starke Kälte hemmt erst die Bildung der Phaeo-, dann der
Eumelanine und führt schliesslich zur weissen ‘‘Polarfärbung’’.
Which can be translated as:
Gloger’s Rule. The melanins in warm-blooded animals
(perhaps in all animals) experience an increase with higher
temperature and humidity. High levels of melanin deposition
lead to the development of iridescent microstructure in
feathers (interference colours).
Dry, hot climate increases only [the deposition of]
phaeo-melanins (yellow, ‘desert-colour’ oxidated), while [the
deposition of] eu-melanins decreases. Strong cold first
inhibits the formation of phaeo-, and then of eu-melanins
and leads finally to white ‘polar colouration’.
Rensch (1936, p. 283) himself subsequently defined
Gloger’s rule in English as follows: ‘In formulating Gloger’s
rule the fact was noted that within a Rassenkreis of warm-blooded
animals the races living in warmer and wetter regions show more
pigmentation by melanins than the races of colder and drier regions, and
that furthermore in hot and dry zones the light brown melanins prevail,
which inversely diminish in cold regions.’ Note, with ‘Rassenkreis’
Rensch refers to a complex of races within a species (Rensch,
1936).
A similar definition was used by Ernst Mayr (Mayr, 1942,
p. 90): ‘Gloger’s Rule. –The melanins increase in the warm and
humid parts of the range. Reddish or yellowish-brown phaeomelanins
prevail in arid climates where the blackish melanins are reduced. The
phaeomelanins are subject to reduction in cold climate, and in extreme
cases also the eumelanin (polar white).’
A few points merit mention here. First, the rule is rather
complicated and comes in two versions. A simple version
referring to melanin in general, and a more complex version
highlighting the different climatic effects on the two types of
melanin: eu-melanins increase with humidity, and decrease
only at extreme low temperatures, while phaeomelanins
prevail in dry and warm regions and decrease rapidly
with low temperatures (Fig. 1). The simple version is not
straightforward either, since it refers to the effects of both
temperature and humidity on melanin deposition, but it is
unclear within the definition whether both need to act in
concert or can have independent effects. This is unfortunate,
because Rensch (Rensch, 1929) mentions in the preceding
sections (p. 156) that the effect of humidity was expected to
be more important than the effect of temperature. Second,
the rule was formulated to describe patterns of intraspecific
variation in colouration of endotherms, although Rensch
leaves open the possibility that it could apply more broadly
to all animals. Third, when formulated the rule had no
associated mechanisms explaining these climatic effects,
unlike other rules such as Bergmann’s rule, where the
A review of Gloger’s rule 1297

Fig. 1. Summary of the simple (A) and the complex (B) versions of Gloger’s rule as defined by (Rensch, 1929) following (Görnitz,
1923). While the simple version (A) predicts increased overall melanin deposition in warm and humid climates the complex version
(B) separates temperature and humidity effects on both main types of melanin deposited in animals: eu-melanin and phaeo-melanin.
Arrows and intensity of colour indicate increased deposition of each pigment with temperature and humidity.

mechanism is considered a clear part of the rule (Salewski &
Watt, 2017) but see (Meiri, 2011; Olalla-Tárraga, 2011). A
complex rule that is not associated with a clear mechanism
is a good candidate for confusion, as we shall see below.
III. HOW IS GLOGER’S RULE DEFINED IN THE
LITERATURE?
To determine how Gloger’s rule is used and defined in the
literature I carried out a Google Scholar full text search on
30 May 2018 with the search term ‘gloger’s rule’ (N = 509
records). Google Scholar search results were exported using
the Publish or Perish software (Harzing, 2007). Google Scholar
searches have the advantage that they include a broader
variety of sources and search within the text when it is
available (Gehanno, Rollin & Darmoni, 2013). This also
identifies studies where the rule is mentioned in the text but
not in the key words, abstract or title. One disadvantage is
that this search engine shows higher temporal variation in
the number of search hits due to variation in the accessibility
of the underlying databases, and hence the outcomes of the
same search may vary at different times (Bramer, 2016). It is
recommended to combine Google Scholar searches with other
search engines (Haddaway et al., 2015). I therefore repeated
the search on Web of Science (7 June 2018, all databases as
provided by Monash University library, N = 59 records,
‘Timespan: All years. Databases: WOS, BIOABS, BIOSIS,
CCC, DRCI, KJD, MEDLINE, RSCI, SCIELO. Search
language = Auto’). While the combined results from both
searches do not encompass all mentions of Gloger’s rule in the
published literature, nor all climatic effects on colouration,
they do provide a substantial sample of such studies.
Some results (N = 100) were discarded because they were
either citations, patents, duplicates of other results (different
versions of the same paper detected more than once, the same
data used in different papers, or in PhD theses and subsequent
papers), written in a language that I could not read (Japanese,
Estonian, Czech), constituted unsuitable sources (websites,
letters, tables of contents, etc.) or were inaccessible through
the university library (Fig. 2). This yielded a total of 422
results that were read and searched for references to Gloger’s
rule. Out of these, 105 did not mention Gloger’s rule in
the text [usually because they cited papers with ‘Gloger’s
rule’ in the title, e.g. Burtt & Ichida (2004); Koski &
Ashman (2015)], and 46 only mentioned the rule without
clearly defining it. This yielded a total of 271 studies with
definitions (see online Supporting information, Table S1).
Most definitions (N = 213) came from scientific journals,
followed by books (N = 33), theses (N = 18), and the rest
from avicultural magazines (N = 4), reports (N = 2), and
published conference abstract (N = 1).
Only 19 (7%) definitions resembled (at least in part)
the original complex definition of Gloger’s rule, which
makes different predictions for the two types of melanin.
The rest were mainly concerned with general variation
in pigmentation intensity or simply dark-to-light variation
(Fig. 3A). Seventy (25.8%) definitions were in agreement with
the simple version of Gloger’s rule (see Section II), namely
predicting more pigmented/darker animals in wet and warm
regions (this includes the 18 more complex definitions as
well). The most widespread definition (N = 132, 48.7%)

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1298 Kaspar Delhey

Fig. 2. Flowchart depicting the literature search, screening and data collection process.

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A review of Gloger’s rule 1299

Fig. 3. Graphical representation of the number of studies that refer to different climatic, environmental and geographic variables
in their definitions of Gloger’s rule (A) and number of studies finding support for effects of different climatic, environmental and
geographic variables in qualitative tests of Gloger’s rule (B). The area of circles is directly proportional to the number of studies
mentioning/supporting each variable (numbers depicted in parentheses). Numbers depicted in circle intersection areas represent
studies that mention or support the effects of more than one variable in the definitions or tests, respectively.

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1300
only mentioned the effects of humidity/precipitation stating
that darker or more-pigmented animals are found in wetter
areas. Overall, 223 (82%) definitions predicted darker colours
in more humid environments. Darker colours in warmer
regions were predicted in 81 definitions (29.8%), darker
colours in forested regions in 10 (3.6%), darker colours at
lower latitudes in 22 (8.1%), and darker colours in more sunny
regions or regions with higher ultraviolet (UV) radiation
in two cases. Interestingly, a small proportion (9.6%) of
definitions also predicted patterns that seemingly oppose
the original definition: darker animals at higher latitudes
(3), altitudes (1) or lower temperatures (22). However, no
definitions predicted darker animals in drier regions.
IV. SUPPORT FOR GLOGER’S RULE
In total 167 studies included some test of Gloger’s rule.
Most (124, 74.3%) were qualitative tests, that is, the authors
simply stated that a species or group of species followed
(or not) Gloger’s rule based on patterns of distribution
but without any associated statistical tests (e.g. darker
subspecies found in humid regions). Only 43 studies (25.7%)
could be considered quantitative tests, that is, where
statistical tests were used to assess the correlation between
colour-variation variables and environmental (rainfall,
humidity, temperature, etc.) or geographic (latitude, altitude)
variables. These studies were included in a meta-analysis (see
Section IV.2).
(1) Qualitative tests
Qualitative tests of Gloger’s rule (Table 1) included studies
on birds (N = 70), mammals (N = 31), insects (N = 15),
reptiles (N = 5), amphibians (N = 2), and arachnids
(N = 1). Most of these tests were done at the intraspecific
level (N = 99), the rest across species (N = 25) and in
terms of spatial scale most tests were done at the regional
scale (N = 85), followed by continental scale (N = 26) and
global scale (N = 13). Studies at a global scale referred
to geographic variation that spans multiple continents,
continental scale refers to geographic variation that spans
an entire continent or most of it and regional-scale studies
refer to geographic variation at smaller scales.
Only five studies (4.5%) reported darker colours in wet
and warm regions, in agreement with the simple version of
Gloger’s rule (Fig. 3B). In partial agreement with Gloger’s
rule, the great majority (71%) of studies reported darker
colours in more humid environments, 12% reported darker
colours in warmer regions or at low latitudes and 4% reported
darker colours in more-vegetated regions (Fig. 3B). Contrary
to Gloger’s rule, 9.6% reported darker colours in colder
or higher latitude/altitude regions, 3.2% reported darker
colours in drier regions and 11.2% reported no patterns
of correlation or inconclusive results (Fig. 3B). Note that
these percentages do not add up to 100% because some
studies report links with more than one variable (e.g. darker
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Kaspar Delhey
where warm and wet); for a full breakdown of numbers
see Fig. 3B.
Darker colours in more-humid areas seem to apply across
taxonomic groups as they are the most common reported
pattern in birds (54/70, 77%), mammals (21/31, 67%) and
arthropods (11/16, 68%). Few studies were available for
amphibians and reptiles.
(2) Quantitative tests
(a) Meta-analytical methods
I considered for the meta-analysis all 43 quantitative
studies that tested some aspect of Gloger’s rule. To
quantify the support for Gloger’s rule in its different
interpretations I extracted effect sizes testing the association
between climatic or geographic variables with colouration.
I considered variables that could be grouped as broadly
representative of variation in temperature (average annual
temperature, winter temperature, etc.), humidity (average
rainfall, evapotranspiration, cloud cover, etc.), vegetation
(forest cover, primary productivity, etc.), and radiation
(total solar radiation, UVB radiation, etc.), since these
broad categories were implicated as part of Gloger’s rule
in the literature surveyed (see Section III). In addition, I
also considered the effects of latitude and altitude. The
sample of quantitative studies included analyses carried
out at three different levels: intraspecific (studies testing
associations between intraspecific variation in colouration
and relevant variables), interspecific (comparative analyses
testing associations between colouration and relevant
variables across species) and assemblage level (usually
spatial analyses that quantified the association of average
colouration of assemblages of species living in a particular
location with the corresponding relevant variables). I also
scored the spatial scale of each effect as described above.
Each statistical effect was converted into the standardised
effect Zr, which is recommended for meta-analyses
quantifying an association between variables (Nakagawa
& Cuthill, 2007). Effects converted included correlation
coefficients (r, rs, R2 ; N = 82), and various test statistics
(t, F , z, Chi2 , etc.; N = 155). The sign of each effect was set
as positive if it supported the patterns predicted by Gloger’s
rule or similar definitions (darker colouration in more humid,
vegetated, warmer areas; where solar radiation is higher; or
at low latitude or altitude). Whenever the effects of multiple
variables were tested simultaneously in the same model I
preferentially included those effects instead of their univariate
alternatives. For each study I extracted all possible effects,
and this resulted in some studies contributing more than one
effect. Variance of Zr was computed as 1/(N –3) following
Nakagawa & Cuthill (2007), where N is sample size. For
seven effects (four studies) there was insufficient information
to compute standardised effect sizes (no direction of effect,
or no further detail on non-significant effects). Following
Booksmythe et al. (2017) I adopted a conservative approach
and assigned an effect of 0 to missing effects and an effect
opposing the predictions of Gloger’s rule when only the sign
A review of Gloger’s rule 1301

Table 1. Summary of the list of studies that provide qualitative tests of Gloger’s rule as detected by the literature search.
Nomenclature follows the names given in each study.

Taxonomic group Taxon/taxa Level Darker where: Reference

Reptiles Florida scrub lizard (Sceloporus woodi) Intraspecific Closed vegetation Jackson (1973)
Reptiles Dasypeltis snakes Interspecific Wet Gans (1961)
Reptiles Lizards Interspecific Unclear/no pattern Hutchinson & Larimer
(1960)
Reptiles Lizards Interspecific Unclear/no pattern Cowles (1958)
Reptiles Snakes Intraspecific High latitude Smith (1956)
Amphibians Wood frog (Rana sylvatica) Intraspecific Unclear/no pattern Martof & Humphries
(1959)
Amphibians Bufo mauritanicus Intraspecific Wet Schneider (1978)
Birds Jerdon’s babbler (Chrysomma altirostre) Intraspecific Wet Sadanandan et al.
(2018)
Birds Larks (Alaudidae) Interspecific Wet Donald et al. (2017)
Birds Flameback woodpeckers (Dinopium Interspecific Wet Ranasinghe &
psarodes and D. benghalese) Seneviratne (2017)
Birds Wood pigeon (Columba palumbus) Intraspecific Wet Cataldo (2017)
Birds Plain wren (Cantorchilus modestus) Intraspecific Wet Saucier et al. (2015)
Birds Narrow-billed woodcreeper Intraspecific Wet Leguizamon & Silveira
(Lepidocolaptes angustirostris) (2015)
Birds Hairy (Picoides villosus) and downy Intraspecific Wet Prum (2014)
(P. pubescens) woodpeckers
Birds Red-legged tinamou (Crypturellus Intraspecific Wet Laverde & Cadena
erythropus) and brown tinamou (2014)
(C. obsoletus)
Birds Automolus foliage-gleaners and allies Interspecific Wet+forest Claramunt et al. (2013)
(Furnariidae)
Birds Buff-breasted earthcreeper (Upucerthia Intraspecific Wet Areta & Pearman
validirostris) (2013)
Birds Long-tailed cinclodes (Cinclodes pabsti) Interspecific Dry Freitas et al. (2012)
and cipo cinclodes (C. espinhacensis)
birds Sage sparrow (Artemisiospiza belli) Intraspecific Wet Cicero & Koo (2012)
Birds Scaled-throated earthcreeper (Upucerthia Interspecific Wet Areta & Pearman
dumetaria) and patagonian forest (2009)
earthcreeper (U. saturatior)
Birds Turkey (Melleagris gallopavo) Intraspecific Wet Speller (2009)
Birds Galerida larks Interspecific Wet Guillaumet et al. (2008)
Birds Bearded vulture (Gypaetus barbatus) Intraspecific Unclear/no pattern Margalida et al. (2008)
Birds Malagasy scops-owl (Otus rutilus) Intraspecific Wet Fuchs et al. (2007)
Birds Papuan frogmouth (Podargus papuensis) Intraspecific Wet Schodde (2005)
Birds Song sparrow (Melospiza melodia Intraspecific Wet Patten et al. (2004)
heermanni and M. m. fallax)
Birds Altai gyrfalcon (Falco altaicus) and saker Interspecific Cold Moseikin & Ellis (2004)
falcon (F. cherrug)
Birds Great pampa finch (Embernagra platensis) Intraspecific Wet Hayes (2003)
Birds Peregrine falcon (Falco peregrinus Intraspecific Wet+warm Döttlinger (2002)
peregrinator)
Birds Suiriri flycatcher (Suiriri suiriri) Intraspecific Eet Hayes (2001)
Birds Black-breasted puffleg (Eriocnemis Intraspecific High altitude Schuchmann et al.
nigrivestis) (2001)
Birds Hawaiian rail (Porzana sandwichensis) Intraspecific Wet Olson (1999)
Birds Splendid fairy wren (Malurus splendens) Intraspecific Wet Cairns & Smith (1999)
Birds Eastern rosella (Platycercus eximius) Intraspecific Wet De Graaff (1998)
Birds Crimson rosella (Platycercus elegans) Intraspecific Wet + warm Hyde (1998)
Birds Slaty antshrike (Thamnophilus punctatus) Intraspecific Wet Isler et al. (1997)
Birds Woodcreepers (Dendrocolaptes spp.) Interspecific Wet Marantz (1997)
Birds Variable seedeater allospecies (S. corvina, Interspecific Wet Stiles (1996)
S. intermedia, S. murallae, and S.
americana)
Birds American robin (Turdus migratorius) Intraspecific Wet Aldrich & James (1991)

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1302 Kaspar Delhey

Table 1. continued

Taxonomic group Taxon/taxa Level Darker where: Reference

Birds Puffinus shearwaters Interspecific Cold Yésou et al. (1990)
Birds New Zealand bellbird (Anthornis Intraspecific Cold Bartle & Sagar (1987)
melanura)
Birds Giant conebill (Oreomanes fraseri) Intraspecific Wet Vuilleumier (1984)
Birds Peregrine falcon (Falco peregrinus) Intraspecific Wet + cold Olsen (1982)
Birds Orioles (Oriolidae) and friarbirds Interspecific Unclear/no pattern Diamond (1982)
(Meliphagidae)
Birds Striated heron (Butorides striatus) Intraspecific Unclear/no pattern Schodde et al. (1980)
Birds Australian chats (Epthianura spp.) Interspecific Wet Williams (1979)
Birds Guineafowl (Numididae) Intraspecific Unclear/no pattern Crowe (1978)
Birds Little shrikethrush (Colluricincla Intraspecific Wet Schodde & Mason
megarhyncha) (1976)
Birds White-throated grasswren (Amytornis Interspecific Wet Schodde & Mason
woodwardi) & Carpentarian grasswren (1975)
(A. dorotheae)
Birds Yellow-tufted honeyeaters (Meliphaga Intraspecific Wet Crome (1973)
melanops/cassidix)
Birds Eastern bluebird (Sialia sialis) Intraspecific Dry Webster (1973)
Birds Merlin (Falco columbarius) Intraspecific Wet Temple (1972)
Birds Ant tanagers (Habia) Interspecific Wet Willis (1972)
Birds Giant petrel (Macronectes giganteus) Intraspecific Unclear/no pattern Shaughnessy (1971)
Birds Hermit thrush (Catharus guttatus) Intraspecific Wet Aldrich (1968)
Birds Tasmanian birds Intraspecific Wet Ridpath & Moreau
(1966)
Birds Quelea (Quelea quelea) Intraspecific Wet + cold Ward (1966)
Birds Purple martin (Progne subis) Intraspecific Wet Johnston (1966)
Birds 19 Passerines and their continental Interspecific Dry Grant (1965)
counterparts
Birds Screech owl (Otus asio) Intraspecific Wet Owen (1963)
Birds Rose-throated becard (Platypsaris aglaie) Intraspecific Wet Webster (1963)
Birds Western yellow robin (Eopsaltria Intraspecific Unclear/no pattern Ford (1963)
griseogularis)
Birds Yellow-tufted honeyeater (Meliphaga Intraspecific Wet Wakefield (1958)
melanops)
Birds Weebill (Smicrornis brevirostris) Intraspecific Wet Keast (1958)
Birds Yellow-throated miner (Manorina Intraspecific Wet Brown & Wilson (1956)
flavigula)
Birds Rough-legged hawk (Buteo lagopus) Intraspecific Wet Cade (1955)
Birds 50 Species of Malaysian birds Intraspecific Wet Longhurst (1951)
Birds Jays (Aphelocoma caeroulescens & A. Intraspecific Wet Farner (1952)
ultramarina)
Birds Darwin’s finches Interspecific Unclear/no pattern Lack (1983)
Birds Peregrine falcon (Falco peregrinus) Intraspecific Wet White & Boyce (1988)
Birds North American birds Intraspecific Wet Zink & Remsen (1986)
Birds South African birds Intraspecific Wet Macdonald (1957)
Birds Nepalese birds Intraspecific Wet Ripley (1950)
Birds Genus Vireo Intraspecific Wet Hamilton (1958)
Birds Grey-crowned woodpecker (Piculus Intraspecific Low latitude Baptista (1978)
auricularis) and golden-olive
woodpecker (P. rubiginosus)
Birds Redpoll complex (Carduelis Interspecific Warm Marthinsen et al. (2008)
flammea–hornemanni–cabaret)
Birds Bluewinged parrotlet (Forpus Intraspecific Wet Bocalini & Silveira
xanthopterygius) (2015)
Mammals Felidae Intraspecific Wet + forest Seidensticker &
Lumpkin (2016)
Mammals Southern birch mice (Sicista subtilis Intraspecific Wet Cserkész et al. (2016)
group)

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A review of Gloger’s rule 1303

Table 1. continued

Taxonomic group Taxon/taxa Level Darker where: Reference

Mammals Human (Homo sapiens) Intraspecific Low latitude Osborne & Hames
(2014)
Mammals Geoffroy’s cat (Leopardus geoffroyi) Intraspecific Low latitude Nascimento (2014)
Mammals Mammals Interspecific Wet/forest/low latitude Caro (2013)
Mammals LaVal’s myotis (Myotis lavali) Intraspecific Wet Moratelli & Wilson
(2013)
Mammals Israeli subterranean blind mole rat Intraspecific Wet Singaravelan et al.
(Spalax ehrenbergi) (2013)
Mammals Spiny mouse (Acomys cahirinus) Intraspecific Wet Singaravelan et al.
(2010)
Mammals Big brown bat (Eptesicus fuscus) Intraspecific Wet Hoffman & Genoways
(2008)
Mammals Mammals Interspecific Low latitude Caro (2005)
Mammals Wolf (Canis lupus) Intraspecific Low latitude Gipson et al. (2002)
Mammals Chipmunks (Tamias senex and T. siskiyou) Intraspecific Wet Sutton & Patterson
(2000)
Mammals Humpback whale (Megaptera novaeangliae) Intraspecific Low latitude Allen et al. (1994)
Mammals Slender mongoose (Galerella sanguinea) Intraspecific Wet Watson (1990)
Mammals Subterranean mole rats (Spalax ehrenbergi Intraspecific Wet Heth et al. (1988)
superspecies)
Mammals Human (Homo sapiens) Intraspecific Unclear/no pattern Fernandez (1984)
Mammals Doria’s tree-kangaroo (Dendrolagus Intraspecific Wet Groves (1982)
dorianus)
Mammals Subterranean mammals Interspecific Wet Nevo (1979)
Mammals Chipmunk (Eutamias obscurus complex) Intraspecific Wet Callahan (1976)
Mammals North American badger (Taxidea taxus) Intraspecific Wet Long (1972)
Mammals Spermophilus ground squirrel (S. beldingi) Intraspecific Wet Turner (1972)
Mammals Insectivores Intraspecific Unclear/no pattern Abe (1967)
Mammals Great basin pocket mouse (Perognathus Intraspecific Wet + cold Iverson (1967)
parvus)
Mammals Mammals Interspecific Unclear/no pattern Hock (1965)
Mammals Mammals Intraspecific Unclear/no pattern Foster (1963)
Mammals Crocidura shrews Intraspecific Wet Meester (1963a)
Mammals Shrew (Crocidura hirta) Intraspecific Wet Meester (1963b)
Mammals Shrew (Crocidura hirta) Intraspecific Wet + warm Meester (1959)
Mammals Brush possum (Trichosurus vulpecula) Intraspecific Wet Guiler & Banks (1958)
Mammals Cattle (Bos taurus) Intraspecific Low latitude Hammond (1954)
Mammals Marten (Martes americana) Intraspecific Wet Hagmeier (1963)
Insects Lacewing (Chrysoperla affinis) Intraspecific Wet + forest Thierry et al. (2011)
Insects Pomarea monarchs Intraspecific Wet Cibois et al. (2004)
Insects Honey bee (Apis mellifera) Intraspecific Cold Ruttner (1988)
Insects Porocara beetles Interspecific Wet Baehr (1986)
Insects Diphlebia damselflies Intraspecific Wet + warm Stewart (1982)
Insects Soldier beetle (Chauliognathus proteus) Intraspecific Wet + cold Miskimen (1972)
Insects Stilt-legged fly (Compsobata mima) Intraspecific Wet+high altitude Merritt (1970)
Insects Horse fly (Tabanus frontalis) Intraspecific High latitude Mcalpine (1961)
Insects Monarch butterfly (Danaus plexippus) Intraspecific Wet + warm Urquhart (1960)
Insects Midge (Culicoides variipennis) Intraspecific Wet Wirth & Jones (1957)
Insects Ant (Formica oregonensis) Intraspecific Low latitude Cole (1956)
Insects Solitary bee (Hoplitis albifrons) Intraspecific Dry + warm Michener (1947)
Insects Insects Intraspecific Wet Dobzhansky (1944)
Insects Coccinelidae Intraspecific Wet Dobzhansky (1933)
Insects Dragonfly (Libellula luctuosa) Intraspecific Cold Garrison (1976)
Arachnids Spider (Loxosceles spinulosa) Intraspecific Wet Newlands (1975)

of the effect was missing. For four effects (four studies) I Schueler, 1982; da Silva et al., 2016, 2017). But since in
could not extract a standardised effect due to the nature all cases the authors concluded that the results supported
of the analyses (climate niche modelling, structural equation Gloger’s rule, I decided to exclude these studies rather than
modelling, canonical correlations; Watson & Hanham, 1976; assign them an effect of 0. Finally, I excluded one study

Biological Reviews 94 (2019) 1294–1316 © 2019 Cambridge Philosophical Society

1304
(Koski & Ashman, 2015) because it concerned plants and the
pigments involved were flavonoids and not melanin. This
yielded a total of 241 effects (38 studies) included in the
meta-analyses (Table 2).
I carried out random-effect multilevel meta-analyses,
using the package MCMCglmm (Hadfield, 2010). Random
effects included taxon identity [some taxa were included in
different studies, for example Tyto owls (Roulin, Wink &
Salamin, 2009; Roulin & Randin, 2015)] and a higher-level
indicator of taxonomic relatedness (usually taxonomic order).
Ideally, it would be better to control for phylogenetic
relatedness, however this was not possible due to the different
levels at which the analyses took place, which included
intraspecific (N = 134 effects), interspecific (N = 70 effects)
and assemblage-level analyses (N = 37 effects). Study ID
was not included since it largely overlapped with taxon
identity, as 47 out of 48 taxa were represented by only one
study. I used normal distributions centred on zero with large
variances as priors for fixed effects, parameter-expanded
priors for the random effects and inverse gamma priors for
the residuals. Each model was run over 1,001,000 iterations,
with a burn in and a thin interval of 1000, resulting in a
posterior sample of 1000. Model convergence was assessed by
examining trace plots and autocorrelation plots. I computed
heterogeneity as I 2 following Nakagawa & Santos (2012).
Funnel plots were used to detect publication bias, together
with Egger’s test (Stuck et al., 1998) and trim-and-fill methods
(both L0 and R0; Duval & Tweedie, 2000) as implemented
in the package metafor (Viechtbauer, 2016). These tests were
carried out on the meta-analytical residuals since these are
statistically independent units that account for the effects
of potential moderators (Nakagawa & Santos, 2012). All
analyses were carried out within the R statistical environment
(R Development Core Team, 2014).
(b) Meta-analytical results
Overall, across all types of environmental effects,
the meta-analysis revealed some support for predictions
based on Gloger’s rule: the meta-analytical mean was
positive yet the 95% credible interval was broad and slightly
overlapped 0 (Table 3, Fig. 4). Based on benchmarks, this
should be considered a small effect (Nakagawa & Cuthill,
2007). However, while Egger’s test indicated no funnel plot
asymmetry in model residuals suggestive of publication bias
(Table 3), trim and fill identified 45 studies missing on the left
side of the funnel (Table 2). Taking these into consideration
shifts the meta-analytical mean substantially, which becomes
even smaller (Table 3, Fig. 4). This lack of overall effect could
be due to combining widely different environmental effects.
Indeed, including type of environmental effect (i.e. latitude,
altitude, humidity, temperature, radiation, vegetation) as a
fixed effect in the model improved model fit as indicated
by a reduction in the Deviance Information Criterion (DIC)
a Bayesian equivalent of Akaike’s Information Criterion
(DIC = −37). Given that effect sizes and signs differed
across environmental variables (Fig. 4), and that we are
mainly interested in humidity and temperature because these
Biological Reviews 94 (2019) 1294–1316 © 2019 Cambridge Philosophical Society
Kaspar Delhey
are the variables included in the original definition, I analysed
the support for each variable separately and determined the
sensitivity of these effects to publication bias as identified by
Egger’s tests and trim-and-fill methods.
These analyses revealed positive effects of humidity,
vegetation, solar radiation, and latitude, and negative
effects of altitude and temperature, although only humidity
and vegetation effects were statistically significant (Table 3,
Fig. 4). Egger’s test identified some level of funnel asymmetry
in the residuals of the humidity model and the trim and fill
identified 2–3 missing studies on the left side. However, the
significant positive effects of humidity remained statistically
significant after accounting for publication bias (Table 3,
Fig. 4). Some of the other environmental effects seemed to
show some levels of funnel plot asymmetry as identified using
the trim-and-fill procedure and this further reduced their
effect sizes (Fig. 4). Heterogeneity due to taxon identity was
moderate to high, while heterogeneity at higher taxonomic
level was lower (Table 3).
Finally, I further tested the generality of humidity and
vegetation effects by including the moderator variables taxon
type, level of analysis and spatial scale. These analyses did not
detect any significant differences in humidity or vegetation
effects across taxonomic groups (birds, mammals, insects),
level of analysis (intraspecific, interspecific or assemblage) or
spatial scale (regional, continental, global), suggesting that
these effects apply broadly (Fig. 5, although note that sample
sizes for vegetation effects were relatively small).
V. DISCUSSION
My survey indicates that there is substantial confusion in the
literature regarding the formulation of Gloger’s rule, and that
the full original definition (Rensch, 1929) is rarely mentioned.
While clearly undesirable, such confusion is nevertheless
understandable given that the original formulation of the
rule was in German and – more importantly – that the
definition is highly complex and invokes the contribution
of two different types of climatic variables (temperature
and humidity) and two different pigments (eu- and
phaeo-melanins) (Fig. 1).
This complexity probably accounts for the multiple
and varied interpretations of the rule published to date.
These refer to Gloger’s rule as predicting correlations
between colouration and latitude, altitude, temperature,
solar radiation, vegetation and humidity, their surrogates, or
combinations thereof (Fig. 3A). Further confusion is added
by the fact that patterns of geographic variation described
in Gloger (1833) are not necessarily the same as defined
by Rensch (1929) when he proposed Gloger’s rule. Some
of the correlations highlighted by Gloger (1833) refer to
increased pigmentation in the tropics (i.e. at lower latitudes),
and latitude can be seen as a surrogate of a variety of climatic
and environmental variables sparking further flexibility in
the choice of variables.
A review of Gloger’s rule 1305

Table 2. Summary of the 38 studies included in the meta-analysis. Nomenclature follows the names given in each study.

Taxonomic
group Taxon/taxa Level Variables N effects Reference
Birds Accipiter melanoleucus Intraspecific Humidity, temperature 2 Amar et al. (2014)
Birds Rhipidura fuliginosa Intraspecific Altitude, humidity, 3 Atkinson & Briskie (2007)
temperature
Birds Haematopus unicolor Intraspecific Humidity 2 Baker (1974)
Birds Chamaea fasciata Intraspecific Humidity, temperature 4 Bowers (1960)
Birds Regulus satrapa Intraspecific Humidity 1 Chui & Doucet (2009)
Birds Petrophassa albipennis Intraspecific Humidity 1 Crome & Johnstone (1979)
Birds Australian landbirds Interspecific, Humidity, temperature, 24 Delhey (2018)
assemblage vegetation
Birds families Acanthizidae and Interspecific Altitude, humidity, 32 Friedman & Remeš (2017)
Meliphagidae latitude, temperature,
vegetation
Birds Chlorodrepanis virens Intraspecific Humidity 1 Gaudioso-Levita et al.
(2017)
Birds Larus glaucescens/Larus Interspecific Latitude 1 Gay et al. (2009)
occidentalis
Birds Zosterops borbonica Intraspecific Altitude 1 Gill (1973)
Birds Cercomacra tyrannina Intraspecific Humidity 3 Graves (1997)
Birds Passer domesticus Intraspecific Humidity, temperature 10 Packard (1967)
Birds Passerculus sandwichensis Intraspecific Altitude, humidity, 4 Rising et al. 2009)
latitude, temperature
Birds Tyto alba Intraspecific Humidity, temperature 6 Roulin & Randin (2015)
Birds Tyto spp. Intraspecific, Humidity, latitude, 30 Roulin et al. (2009)
interspecific temperature
Birds Owls Interspecific Latitude 4 Roulin et al. 2011)
Birds Cranioleuca antisiensis Intraspecific Humidity 1 Seeholzer & Brumfield
(2017)
Birds Chasiempis sandwichensis, Intraspecific Humidity 21 VanderWerf (2012)
Chasiempsis ibidis
Birds, insects Eastern Australian birds Assemblage Humidity, radiation, 14 Dalrymple et al. (2018)
and butterflies temperature, vegetation
Insects Drosophila melanogaster Intraspecific Altitude, humidity, 10 Bastide et al. (2014)
latitude, radiation,
temperature
Insects Ants Assemblage Temperature 1 Bishop et al. (2016)
Insects Phaulacridium vittatum Intraspecific Altitude, latitude, 6 Harris et al. (2012)
temperature
Insects Silpha longicornis Intraspecific Humidity, temperature 2 Nishikawa (2010)
Insects Coccinella septempunctata Intraspecific Humidity, temperature 4 O’Neill et al. (2017)
Insects Dragonflies Assemblage Altitude, humidity, 6 Pinkert et al. (2017)
temperature
Insects Collembola Assemblage Altitude, latitude 3 Rapoport (1969)
Insects Sericinus montelus Intraspecific Latitude 2 Zheng et al. (2015)
Mammals Protoxerus stangeri Intraspecific Humidity, radiation, 3 Amtmann (1965)
temperature
Mammals Homo sapiens Intraspecific Humidity, latitude, 4 Chaplin (2004)
radiation, temperature
Mammals Primates Interspecific Temperature 1 Kamilar & Bradley (2011)
Mammals Sciurus niger Intraspecific Altitude, humidity, 4 Kiltie (1989)
temperature
Mammals Mus musculus Intraspecific Humidity 1 Lai et al. (2008)
Mammals Didelphis virginiana Intraspecific Humidity, temperature 14 Nigenda-Morales et al.
(2018a)
Mammals Primates Interspecific Latitude 3 Santana et al. (2012)
Mammals Artiodactyls Interspecific Latitude, vegetation 5 Stoner et al. (2003b)
Mammals Lagomorphs Interspecific Humidity, latitude, 3 Stoner et al. (2003a)
vegetation
Mammals Cynictis penicilata Intraspecific Humidity, temperature 3 Taylor et al. (1990)

Biological Reviews 94 (2019) 1294–1316 © 2019 Cambridge Philosophical Society

1306 Kaspar Delhey

Despite this seeming anarchy, most (86%) definitions

95% credible intervals (CI; lb, lower boundary; ub, upper boundary) and associated P values. It also indicates overall sample sizes and replication across all random effects

after accounting for publication bias by the trim-and-fill procedure that identified the most missing studies. All missing studies were found on the left side of the funnel except

CI ub
Table 3. Meta-analytical results including the overall meta-analytical mean and separate means for all climatic, environmental and geographic variables together with their

number of missing studies as estimated by the trim-and-fill procedure using methods L0 and R0. Finally, it includes the adjusted meta-analytical means and their 95% CI
(number of effects, broad taxonomic groups and taxa included), heterogeneity at each level, results from Egger’s test of funnel asymmetry carried out on the residuals and the

0.156
0.154
0.357

0.478
0.534
1.382
0.42
include at least one of the two variables mentioned in
the original definition: temperature and humidity (and its

means & 95%CI

close surrogates). The great majority of these studies refer to

−0.126
−0.265
0.122
0.115
−0.593
−0.192
−1.222
meta-analytical

CI lb
simple patterns of light-to-dark variation in colouration. The
Adjusted complex version of Gloger’s rule was not directly tested in
any paper reviewed here. Such tests are substantially more

0.011
−0.041
0.233

−0.074

0.123
0.27

0.12
Zr
complicated as they would involve quantifying the deposition
for temperature and altitude. For latitude, radiation and altitude I did not include the random effect taxonomic group due to low level of replication.

of both eu- and phaeo-melanin either directly or indirectly

(McGraw, Safran & Wakamatsu, 2005; Galván et al., 2013).
R0
0
5
2
0
1
1
0
Some studies come close however. For example, comparisons
and fill
Trim

of eu- and phaeo-melanin concentrations deposited in the

L0
45
10
3
0
1
0
3
pelage of spiny mice (Acomys cahirinus) in the so-called
‘Evolution Canyon’ in Israel, revealed higher eu- and
0.882

0.016
0.679
0.185
0.118
0.485
lower phaeo-melanin in animals from highly vegetated slope
0.58
P

areas compared to sparsely vegetated areas (Singaravelan

Egger’s test

et al., 2010). However, this was essentially a comparison

−0.149
−0.558
2.443
−0.419
−1.395
−1.592
−0.768

between two means and not a test for an association between

t

environmental variables and pigmentation. Thus, given that

in general the complex version of Gloger’s rule has not been
0.331
0.147

0.547
0.942
0.414
0.891
Taxa

tested, what follows refers to the simple version, which can

0.6

be summarised as predicting darker animals in warmer and

wetter areas, through the increased deposition of melanin.
Taxon.

While most definitions refer to humidity or temperature

group
0.122
0.436
0.101

0.317
NA
NA

NA
Heterogeneity I 2

(and their surrogates) only a quarter (25.8%) of these mention

both variables together, as in the simple version of Gloger’s
rule (Fig. 3A). By far the majority of definitions refer to darker
Residual
0.547
0.417
0.299
0.453
0.058
0.269
0.109

animals in more humid environments, without referring

to temperature effects. This preponderance of humidity
effects on dark-to-light variation is echoed by qualitative
and quantitative tests of Gloger’s rule which suggest that
Taxa

humidity effects on colouration (and those of vegetation,

48
24
32
8
10
21
5

which is closely linked to water availability) have high

levels of support, are taxonomically widespread and apply
Taxon.
group

at different scales of analysis (Figs 3B and 4). This agrees

19
14
15
5
6
10
5

with Allen’s observations on North American birds and

Sample sizes

mammals 150 years ago (Allen, 1874), where he suggested

Effects

that humidity effects were stronger than temperature effects,

241
47
97
27
16
48
6

as also suggested by Rensch (1929).

Conversely, temperature effects were not significantly
different from zero (Fig. 4), and in fact many studies show that
0.118
0.206
0.001

0.732
0.402
0.01

0.65
P

the effects of temperature are the opposite of those predicted

by Gloger’s rule (darker animals in colder environments; see
also Rapoport, 1969; Zeuss et al., 2014; Pinkert, Brandl &
means & 95% CI

CI ub
0.259
0.068
0.365

0.475
0.552
1.457
Meta-analytical

0.42

Zeuss, 2017; Delhey, 2018; Galván, Rodríguez-Martínez

& Carrascal, 2018; Heidrich et al., 2018). This pattern
is consistent with another ecogeographical rule, namely
0.114 −0.023
Temperature −0.128 −0.351
0.129
0.115
−0.077 −0.596
0.139 −0.174
0.198 −1.147
CI lb

Bogert’s rule, also called the thermal melanism hypothesis

(Clusella Trullas, van Wyk & Spotila, 2007), which predicts
darker animals in colder regions, chiefly for thermoregulatory
0.241
0.27
Zr

reasons. Thus, it is possible that temperature effects

as predicted by Gloger’s rule are opposed by Bogert’s
rule and this makes detecting temperature effects harder.
Alternatively, the existence of an ecogeographical rule that
Vegetation

Radiation
Humidity

Latitude

predicts the opposite of Gloger’s rule may facilitate the

Altitude
Overall

publication of results that contradict Gloger’s rule. Thus,

it is possible that temperature effects are even more in

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A review of Gloger’s rule 1307

Fig. 4. Forest plot depicting the effects (Zr) of different climatic, environmental and geographic variables on colouration. Each effect
is depicted with its 95% credible interval (CI), except for a large negative altitude effect which is omitted for graphical purposes (but
was included in the analyses). Positive effects support predictions of Gloger’s rule. Different symbol shapes and colours represent
different levels of analysis and taxa, respectively. Meta-analytical means are depicted before (black symbols) and after (grey symbols)
correcting for publication bias using the trim-and-fill method (see Table 3). The overall meta-analytical mean across all effects is
depicted at the bottom of the graph as a diamond, and separate meta-analytical means are also given for each category of climatic,
environmental or geographic effect.

disagreement with Gloger’s rule than shown here. On the
other hand, since there is no rule predicting darker colours in
drier environments, studies finding such patterns may be less
likely to be published, resulting in publication bias favouring
the humidity aspect of Gloger’s rule.
The meta-analysis also revealed effects of latitude and solar
radiation consistent with some definitions of Gloger’s rule
(although these were not statistically significant Fig. 4). The
effects of latitude agree with Gloger’s predictions of darker
tropical birds and mammals (Gloger, 1833), and observations
on the colouration of birds in North and Central America
(Bailey, 1978). These latitudinal patterns, while intriguing,
are not very illuminating since many climatic/environmental
variables can vary with latitude, and are often strongly
correlated with each other. Beyond the obvious correlation
between latitude and temperature, one such variable is the
amount of solar radiation, in particular UV radiation, which
is also higher close to the equator. Increased pigmentation in
these circumstances has been seen as protective against the
harmful effects of UV, something that seems to be supported
to some extent in humans (Chaplin, 2004; Jablonski &
Chaplin, 2017), fruit flies (Bastide et al., 2014) and by
experimental evidence in plants (Koski & Ashman, 2015).
This last result in particular has been interpreted as providing
fresh insights into the mechanisms behind Gloger’s rule
(Cuthill, 2015). However, the pigments involved are not
melanins but flavonoids (Koski & Ashman, 2015). Since
Gloger’s rule clearly refers to the deposition of melanin, this
study and others on plants (Watson & Hanham, 1976) may
not constitute good examples of the rule, which was explicitly
formulated for animals (Rensch, 1929).
Complex definitions combined with ambiguous use and
only partial empirical support may be indicative that Gloger’s
rule should be declared invalid or, at least, reformulated.
Strictly speaking, current evidence suggests that the simple
version of Gloger’s rule as formulated by Rensch (1929) does
not seem to be valid, since the meta-analysis provides no
support for the expected temperature effect. Alternatively,
Gloger’s rule could be reformulated to include only the
effects of humidity (darker where wet), which, according
to my survey, seems to be the definition endorsed by most
researchers (Fig. 3A) and the one that is best supported by the
evidence (Fig. 3B and 4). While this would be probably the
preferred option, the current meta-analytical results should
only be seen as a starting point for more rigorous testing, as
it is possible that publication biases are considerably more
important than quantified here.
Future tests of Gloger’s rule should aim at collecting
new data on colour variation (for example using museum
specimens; Little et al., 2017) via randomised designs to avoid

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1308 Kaspar Delhey

Fig. 5. Forest plot depicting the contrasts (Zr) between the levels of three moderator factors [broad taxonomic group (birds,
mammals or insects), level of analysis (intraspecific, interspecific or assemblage) and spatial scale (regional, continental or global)]
corresponding to the effects of humidity and vegetation on animal colouration. Depicted are mean differences and their 95% credible
intervals for each contrast. In all cases 95% credible intervals overlap zero indicating that none of these contrasts is statistically
significant. There were no effects of vegetation at the intraspecific level and hence these contrasts are not shown.

choosing specific taxa or specimens. The colour variation
measured should be consistent with variation in melanin
deposition, and ideally melanin concentrations should be
measured directly (Singaravelan et al., 2010; Galván &
Wakamatsu, 2016). These studies should clearly define what
version of Gloger’s rule is being tested, and quantify the effects
of both temperature and humidity. Such studies should focus
not only on birds and mammals, but on other groups as well,
since the original definition explicitly acknowledges that the
rule could apply more broadly and my meta-analytical results
suggest that humidity effects also apply to insects. Studies
should also encompass all levels of variation from intraspecific
to assemblage level and a broad range of spatial scales
(Gaston, Chown & Evans, 2008), as humidity effects seem
to apply across different levels and spatial scales (Fig. 5). In
addition, we need well-designed studies that test the different
adaptive and non-adaptive mechanisms that could explain
the patterns described by Gloger’s rule since, as indicated
for Bergmann’s rule, a proper ecogeographical rule should
be based on a clear mechanism (Watt & Salewski, 2011;
Salewski & Watt, 2017).
In this regard, redefining Gloger’s rule in terms of humidity
and refocusing colour variation on the contribution of
melanin pigments provides an opportunity to re-assess the
most likely mechanisms behind these patterns. Moreover,
advances in knowledge on the biochemistry, metabolism,
genetic basis and function of melanin pigments (Ducrest,
Keller & Roulin, 2008; Wittkopp & Beldade, 2009;
Roulin & Ducrest, 2011, 2013; Solano, 2014; Galván &
Solano, 2016; Cordero & Casadevall, 2017) provide fresh
insights to define plausible mechanisms. This was already
recognised by Rensch (1929) as essential to understanding the
underpinnings of the rule. Four main mechanisms have been
proposed: camouflage (Zink & Remsen, 1986), protection
against parasites (Burtt & Ichida, 2004), protection against
UV radiation (Koski & Ashman, 2015) and pleiotropic effects
(Ducrest et al., 2008). As indicated above, the effects of solar
or UV radiation do not have consistent support (Fig. 4) and
hence this mechanism is unlikely to be a general explanation.
Hence, below I will focus on the other three mechanisms to
explain the link between colouration and humidity (and its
surrogates).

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A review of Gloger’s rule
Camouflage is probably the most commonly invoked
mechanisms behind Gloger’s rule (Zink & Remsen, 1986;
Delhey, 2017), and is attractive as a general explanation since
it would apply broadly, as it is relevant not only to birds and
mammals but also to animals in general. Darker animals in
more humid regions would be better camouflaged because
these harbour more dense vegetation which blocks light and
often have soils rich in organic matter resulting in shaded
environments with dark backgrounds.
While the importance of background matching in terms
of camouflage is well established (Cuthill et al., 2017), there
are few studies that have assessed this in the context of
gradients in humidity or vegetation. A recent experimental
study using butterfly models showed that darker models
have higher ‘survival’ than light models within forests
but not in open environments, and this matches natural
variation in butterfly colours (Cheng et al., 2018). Other
experimental studies have revealed the importance of
background colour matching using rodent models, although
not along humidity or vegetation gradients but gradients of
soil colour (Mullen & Hoekstra, 2008). The fact that animal
colouration often changes abruptly to match background
colouration on a very small spatial scale and unrelated to
climatic variability, has been used to cast doubt on the
generality of Gloger’s rule (Lomolino et al., 2006). However,
the existence of consistent geographic patterns of variation
along humidity gradients (Fig. 4) suggests that, while such
small-scale spatial variation may weaken climatic effects,
camouflage cannot be ruled out as a driving force behind
darker animals in more humid environments. Ideally, testing
the camouflage hypothesis should be done experimentally
using models depicting realistic patterns of colour variation
as observed along previously identified climatic gradients
at different spatial scales and quantifying their ‘survival’.
In this regard, widespread access to three-dimensional (3D)
printers will allow the deployment across different climatic or
environmental gradients (Cain et al., 2019) of large numbers
of models with realistic colours based on the visual abilities
of predators (Delhey et al., 2015).
Alternatively, darker colours due to increased melanin
deposition may be caused by interactions with parasites or
pathogens. Resistance against parasites as an explanation for
Gloger’s rule, in particular darker colours in more humid
areas, was first proposed in the context of protection of
plumage against feather-degrading bacteria (Burtt & Ichida,
2004). Melanin deposition strengthens feathers (Bonser,
1994) and in vitro tests indicate that melanised feathers are
generally [but not always (Grande, Negro & Torres, 2004)]
more resistant to degradation by keratinolytic bacteria (Burtt
& Ichida, 2004; Gunderson et al., 2016; Goldstein et al., 2004).
Moreover, bacteria from humid environments seem to have
higher keratinolytic abilities than strains from arid regions
(Burtt & Ichida, 2004). However, there is little evidence
that keratinolytic bacteria have measurable effects on the
plumage of live birds (Cristol et al., 2005; but see Leclaire
et al., 2014). A further limitation is that this mechanism
would be restricted to birds. It is unclear whether bacterial
Biological Reviews 94 (2019) 1294–1316 © 2019 Cambridge Philosophical Society
1309
degradation of hair or fur is an issue in mammals and it
certainly does not seem to apply to other vertebrates or
arthropods. Parasites and disease could however be linked
with variation in melanin-based colouration in a different
manner, and this brings us to the pleiotropy hypothesis.
The pleiotropy hypothesis was inspired by advances on
the genetic underpinnings of melanin-based colouration
(Mundy, 2005). In particular, genes coding for melanocortin
receptor (MC1R) and its ligands, which affect the deposition
of melanin pigments, can also have other phenotypic effects
(Ducrest et al., 2008). Specifically, it has been predicted
that these pleiotropic effects lead to darker animals having
higher levels of sexual activity, being more aggressive and
less sensitive to stress, having better anti-inflammatory,
antipyretic and anti-oxidative responses, and better energy
balance (Ducrest et al., 2008). If some of these traits are
being selected along humidity gradients this could mean
that gradients in melanin-based colouration may simply be
a by-product of those selection forces.
One such plausible selection force could be an increase
in the prevalence of parasites and pathogens in more humid
or vegetated environments (Moyer et al., 2002; Guernier,
Hochberg & Guégan, 2004; Dunn et al., 2010; Sehgal
et al., 2011; Becker et al., 2012). Such gradients, if general
enough, would favour stronger immune responses in humid
environments (Horrocks et al., 2015) and indirectly (through
pleiotropic effects) higher melanin deposition. However,
whether more-melanised individuals are generally more
immunocompetent remains to be conclusively shown (Cote
et al., 2018). While these predictions have been derived with
vertebrates in mind (Ducrest et al., 2008), the role of melanin
in immunity is even more straightforward in arthropods.
In insects for example, more-melanised individuals often
have higher immune competence, and melanin is used to
encapsulate pathogens (Wittkopp & Beldade, 2009). Thus,
darker animals in more humid environments due to selection
for increased immunocompetence could constitute a general
explanation for Gloger’s rule.
Finally, one possibility that has not received much
attention may link Gloger’s rule with the thermal melanism
hypothesis (Clusella Trullas et al., 2007). Recent work reveals
that this rule may apply to both ectotherms (Clusella-Trullas
et al., 2008; Bishop et al., 2016; Pinkert et al., 2017; Heidrich
et al., 2018) and endotherms (Friedman & Remeš, 2017;
Dalrymple et al., 2018; Delhey, 2018; Galván et al., 2018)
and that the thermoregulatory functions of melanin may be
phylogenetically conserved across the tree of life (Pinkert
& Zeuss, 2018). This rule predicts darker, more-melanised
individuals in colder regions, which would benefit from
absorbing more solar radiation to warm up. Conversely,
lighter, less-melanised organisms would be favoured in
warmer areas where absorbing less radiation would be
advantageous to prevent overheating and reduce evaporative
water loss. It is therefore possible that at least in warm regions,
darker organisms can avoid some of these thermoregulatory
costs if they inhabit humid and vegetated environments, since
these are shaded, cooler and have higher water availability.
1310
Hence, organisms in humid and vegetated environments may
be darker simply because such environments may moderate
the effect of colour on thermoregulation (Xing et al., 2016).
To summarise, combining current advances in the
knowledge of melanin form and function with a better
understanding of the underlying climatic effects (i.e. humidity
gradients) will provide further insights into the likely
mechanisms behind Gloger’s rule. These mechanisms are
not mutually exclusive and future work should aim at
disentangling their contributions across different groups
of organisms. Furthermore, establishing the validity and
generality of Gloger’s rule is not only an academic
exercise. The ubiquity of melanin-based pigmentation in
nature (Mcgraw, 2006; Delhey, 2015; Galván & Solano,
2016) and the multiple adaptive roles it fulfils (Solano,
2014) means that determining the environmental drivers
associated with its variation will provide knowledge that
applies broadly across most animals and possibly beyond
(Cordero et al., 2018). In particular, the links between
melanin-based pigmentation and essential adaptive processes
such as avoiding predators, combating parasites, and
thermoregulation, make understanding how it will respond
to ongoing and future climate change a priority (Roulin,
2014; Delhey & Peters, 2017; Cote et al., 2018). I hope that
this review provides a first step towards more stringent tests
that clarify the validity and generality of Gloger’s rule.
VI. CONCLUSIONS
(1) Gloger’s rule can be defined in a simple or a complex
way: the simple version predicts higher deposition of
melanin pigments (and hence darker colours) in warmer
and more humid areas. The complex version predicts
that the deposition of phaeo-melanins should decrease with
temperature, while only extreme cold will reduce eu-melanin
deposition. In addition, the deposition of eu-melanin
should decrease with lower humidity, while phaeo-melanin
deposition increases.
(2) When referring to Gloger’s rule it should be made
clear which definition is being used and authors should cite
the appropriate reference. I recommend citing the original
version (Rensch, 1929) or some of the early versions in
English (Rensch, 1936; Mayr, 1942). Citing only Gloger
(1833) would not be appropriate since he did not coin the
rule.
(3) The patterns of colour variation described by Gloger’s
rule are caused by differences in the deposition of melanin
pigments. Geographic patterns of colour variation associated
with climatic variation that are not due to melanin deposition
should ideally not be interpreted as part of Gloger’s rule,
although it is likely that the great majority of the dark-to-light
variation in animal colouration is due to differential melanin
deposition.
(4) Based on qualitative and quantitative evidence it
seems that patterns predicted by Gloger’s rule are mainly
Biological Reviews 94 (2019) 1294–1316 © 2019 Cambridge Philosophical Society
Kaspar Delhey
associated with variation in humidity (darker animals in
wetter environments) but not temperature. Strictly speaking,
this could mean that the simple version of Gloger’s rule is not
valid, at least as originally formulated. A possible solution
would be to reformulate Gloger’s rule in terms of humidity
only, since this is the most widespread interpretation of the
rule and the one best supported by the evidence. However,
this conclusion requires more exhaustive tests to rule out
publication bias issues.
(5) A full re-assessment of Gloger’s rule should identify
and test the mechanistic links between colouration and
climate. Based on this review, the most likely mechanisms
that would lead to higher deposition of melanin in more
humid and vegetated regions, and that can apply across
a broad taxonomic range, are camouflage and protection
against parasites and pathogens. The last effect is most
likely driven by pleiotropic effects. Finally, future studies
should assess the extent to which humidity gradients could
disrupt colour effects on thermoregulation as described by
the thermal melanism hypothesis, and to what extent this
could be contributing to the patterns of colour variation
described by Gloger’s rule.
VII. ACKNOWLEDGMENTS
I thank Anne Peters, Alexandre Roulin, the Assistant Editor
Alison Cooper, and one anonymous reviewer for comments
on the manuscript and Shinichi Nakagawa for advice
on meta-analyses.
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IX. SUPPORTING INFORMATION
Additional supporting information may be found online in
the Supporting Information section at the end of the article.
Table S1. List of studies that provide definitions of Gloger’s
rule.