Marine Biology (2020) 167:15

https://doi.org/10.1007/s00227-019-3625-y

ORIGINAL PAPER

Assessing how body size affects the species‑time relationship

in a shallow marine benthic megafauna community exposed
to a strong hypoxia disturbance
Fabio A. Labra1,2 · Eduardo Hernández‑Miranda3,4   · Renato A. Quiñones3,4

Received: 29 November 2018 / Accepted: 15 November 2019

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract
The species–area relationship (SAR) and the species–time relationship (STR) are two well-established macro-ecological
patterns. Species richness has also been shown to follow a humped relationship with body size, suggesting that SAR and STR
may also depend on body size. We test whether the pattern of increase in the number of species with time varies with species
body size. We analyzed data on carnivorous and scavenger species collected in a shallow marine benthic megafauna com-
munity in Coliumo Bay, Chile. Body size data were tabulated into exponential body size classes using two binning strategies.
Species-level binning represented all individuals of each species by their average body size. Individual-level binning tabu-
lated all data into exponential body size classes, allowing species to potentially occupy multiple size classes. We determined
empirical relationships between body size and species richness, as well as estimated temporal species accumulation curves
(TSAC) and nested species–time relationships (NSTR). We also tested whether the increase of species richness within body
size classes follows either a power-law relationship or a logarithmic function. We find that the number of species increases
with the time span studied, both for a TSAC and in the NSTR, for both species-based and individual-based data, while also
showing a unimodal relationship with body size for both species and individual-based data. Thus, the STR is a general pat-
tern, which depends on body size, despite reproductive seasonal forcing and strong hypoxia disturbance in Coliumo Bay.

Communicated by M. Huettel.
Reviewed by A. Carranza, D. Fa, and A. S. Pacheco.
Electronic supplementary material  The online version of this
article (https​://doi.org/10.1007/s0022​7-019-3625-y) contains
supplementary material, which is available to authorized users.
* Eduardo Hernández‑Miranda
eduhernandez@udec.cl
1
Centro de Investigación e Innovación para el Cambio
Climático (CiiCC), Facultad de Ciencias, Universidad Santo
Tomás, Ejército146, 837003 Santiago, Chile
2
Doctorado en Conservación y Gestión de la Biodiversidad,
Facultad de Ciencias, Universidad Santo Tomás, Ejército146,
837003 Santiago, Chile
3
Programa de Investigación Marina de Excelencia (PIMEX),
Facultad de Ciencias Naturales y Oceanográficas,
Universidad de Concepción, Casilla 160‑C, Concepción,
Chile
4 1995; Brooks et al. 1997; Ulrich and Buszko 2003, 2004)
Interdisciplinary Center for Aquaculture Research (INCAR),
Universidad de Concepción, O’Higgins 1695, Concepción,
Chile
Introduction
Understanding the processes that account for the observed
diversity of ecological systems continues to be a central goal
in ecology (Magurran 1988; May 1988; Rosenzweig 1995;
Ricklefs 2004). One of the most general patterns in ecology
is the species–area relationship (SAR), or the increase in
the number of species with increasing area sampled (Pres-
ton 1960; Rosenzweig 1995). This pattern has been argued
to be one of the few laws of ecology (Lawton 1999), and
has been investigated using different approaches ranging
from observational to experimental and modeling studies
(Preston 1960; Rosenzweig 1995; Leitner and Rosenzweig
1997; Chown et al. 1998; Adler and Lauenroth 2003; Allen
and White 2003; Hurlbert 2006). SARs are very important,
from an applied perspective, for conservation efforts and
have been used to estimate species numbers and identify bio-
diversity hotspots (Myers et al. 2000), as well as to forecast
the loss of species or species extinction (Pimm and Askins
and to identify ecological hotspots (Ulrich 2005; Werner

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 15   Page 2 of 13
and Buszko 2005). Most empirical SARs have been shown
to follow Arrhenius power functions of the form:
S = cAZ , (1)
where S is species richness, A is area sampled, and c and Z
are fitted constants (Arrhenius 1921; Drakare et al. 2006;
Dengler 2009). In addition to the power function, SARs have
also been described using a logarithmic model (Rosenzweig
1995; Dengler 2009):
S = c + Z log (A). (2)
However, it has been pointed out that the number of spe-
cies may also depend on the time period of observation, as
well as on the area sampled (Adler and Lauenroth 2003).
In 1960, Preston proposed that the accumulation of species
with sampling time should follow a similar power function
relationship:
S = cT w . (3)
Again, in this equation, S is species richness, T is time
span of sampling, and c and w are fitted constants; the expo-
nent w of this species–time relationship (STR) has been
argued to show similar values to those found in empirical
SARs (Preston 1960). Empirical assessment of available data
shows that while many observed STRs do follow a power
function (Preston 1960; Adler and Lauenroth 2003; Adler
2004; Adler et al. 2005; Fridley et al. 2006), for some eco-
systems and taxonomic groups, there may be a bias towards
a logarithmic function (White 2004, 2007):
S = c + wlog(T). (4)
A meta-analysis of 984 community time series revealed
that overall there was no particular preference in the fit to
either of these functions (White et al. 2006; White 2007). In
addition, the observed STR exponents show a range of val-
ues that either exceeds the values observed in SARs (Adler
and Lauenroth 2003), or overlaps with the typical range of
SAR slopes with 0.2 < Z < 0.4 (White 2007).
The accumulation of species over time may be explained
by the action of different ecological processes such as spe-
cies turnover arising from local extinction and colonization,
native species range expansion, or successful colonization by
introduced exotic species (Adler and Lauenroth 2003). The
accumulation over short-time scales can be attributed mostly
to increasing cumulative sampling effort (White 2004,
2007). Over ecological time scales (decades to centuries) the
changes in species richness should be driven by colonization
and local extinction of species in response to community
succession, environmental variability, demographic stochas-
ticity, as well as metapopulation and source–sink dynamics
(Adler and Lauenroth 2003; White 2004, 2007). Finally,
over longer time scales, species accumulation responds
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Marine Biology (2020) 167:15
to evolutionary change through speciation and extinction
(Preston 1960; Adler and Lauenroth 2003; White 2004,
2007). Meta-analyses suggest that, on average, ecological
communities seem to transition from sampling to ecological
phases within a time scale of 1–4 years (White 2004, 2007).
Nevertheless, recent work on a Central European stream
fish assemblage studied on 12 sampling occasions spanning
3 years revealed power function STR curves within the range
observed in other studies, predominantly from terrestrial
systems (Erös and Schmera 2010). These results show that
species accumulation in space and time is interrelated, with
the effect of time depending on the area sampled, and the
effect of area depending on the time scale of the study (Adler
and Lauenroth 2003; Adler et al. 2005; McGlinn and Palmer
2009). A firm understanding of the spatial and temporal scal-
ing of biodiversity, therefore, requires joint consideration
of these two components (space and time), leading to the
species–time–area relationship (STAR) (Adler et al. 2005;
Erös and Schmera 2010). It has been shown that, in addi-
tion to the effect of time and area, the number of observed
individuals accounts for the number of species (Palmer and
White 1994; McGlinn and Palmer 2009; Azovsky 2011;
Ulrich et al. 2013). Furthermore, observed species richness
in a community has also been shown to depend on the size
and abundance of the individuals studied (May 1988, Morse
et al. 1985, Siemann et al. 1996, 1999). Hence, the rate of
species accumulation may reflect the effects of body size on
either abundance or the available species pool.
Early studies by May (1988) and Morse et al. (1985)
suggest that species richness, abundance, and body size are
interrelated, implying that any efforts to provide a unifying
theory for these community attributes should consider all
three of them (Morse et al. 1985; May 1988). Indeed, Sie-
mann et al. (1996, 1999) showed that for grassland insects,
the relationship between body size (measured as biovolume),
species richness, and abundance (measured as the number
of individuals) follows a parabola in these three dimensions
(Siemann et al. 1996, 1999). Empirical studies documenting
the trivariate relationship between body size (W), the number
of individuals (I), and species richness (S) have focused on
assemblages of a given taxonomic group, such as terrestrial
arthropods (Morse et al. 1985; Siemann et al. 1996, 1999)
and marine mollusks (Fa and Fa 2002; McClain 2004). In all
these systems, observed trivariate WIS relationships tend to
follow a parabola, with logarithmic transformations of both
abundance and species richness showing a right-skewed uni-
modal pattern with body size, while the number of species
increases as a power function of the number of individuals
(Siemann et al. 1996, 1999; Fa and Fa 2002; McClain 2004).
While most of these studies have focused on single taxo-
nomic groups, recent work on a diverse shallow epibenthic
faunal marine community showed that the trivariate relation-
ship is a general pattern, despite seasonal and inter-annual
Marine Biology (2020) 167:15 Page 3 of 13  15
variability in species composition (Labra et al. 2015). In
light of these studies, it seems reasonable to expect that
body size may also affect the rate of increase in new species
with observation time. Nonetheless, to our knowledge, no
studies have examined the interaction of body size with the
rate of increase in species number through time. Moreover,
most of the published examples on STR focus on taxonomic
assemblages rather than on functional groups or ecological
communities.
In this article, we examine the relative effects of body
size (M) and time (T) on the number of individuals (I) and
species richness (S) in a shallow benthic megafauna (or meg-
abenthic) community. Specifically, we examined how body
size influences the accumulation of species through time by
examining the species accumulation curve (SAC) and the
non-nested species–time relationship (STR) across differ-
ent body size classes. Given that species richness shows a
unimodal dependence on body size, we hypothesize that dif-
ferent body size classes will differ in the rate of species accu-
mulation through time, with modal size classes exhibiting
faster rates of species richness increase relative to smaller
and larger size classes.
Methods
Study area and sampling
Coliumo Bay (36° 32′ S; 72° 56′ W) is a small embayment
with depths shallower than 25  m, dominated mainly by
sandy or sedimentary substrates. Data on benthic megafauna
were collected as part of the research program setup by the
Programa de Investigación Marina de Excelencia (PIMEX)
at the Universidad de Concepción (UDEC), Chile. Sampling
was performed at 3-month intervals, yielding data for Janu-
ary, May, August, and November 2007, and January, April,
Table 1  Observed increase of benthic megafauna species at Coliumo Bay
Relationship Logarithmic: S = c + w log(T)
c w a b
Species − 0.22 ± 0.03*** 5.18 ± 0.45*** 0.94 34.11
accumulation
curve (TSAC)
Nested species– 14.21 ± 0.16*** 5.12 ± 0.30*** 0.87 202.77
time relation-
ship (NSTR)
The table shows the fit of the logarithmic (S = c + w log (T)) and power-law (S = cTw) scaling models to both the Species Accumulation Curve
and the Species–Time Relationship at Coliumo Bay. For each of these relationships the table shows the fitted values of the constant c and species
richness scaling exponent w, with their corresponding standard errors. Also shown are the R2, BIC, and ∆BIC values. Minimum values of BIC
for each row are highlighted in bold, indicating the selected model
Significance levels for the slope parameters are shown by the following abbreviations: ***p < 0.001; **p < 0.01; *p < 0.05; ns: p > 0.05. See text
for details on the meaning of the different parameters
July, and October 2008, and January 2009. Sampling was
carried out using UDEC’s research vessel L/C Kay–Kay II at
three sampling stations within Coliumo Bay, using a modi-
fied Agassiz trawl (1 m wide × 1 m long × 30 cm high lined
with 5 mm “knot-to-knot” netting). Survey distance aver-
aged 378 m ± 145 m of the sea bottom, cruising for 5 min
at 1.5–2 knots. Once collected, biological samples were
washed and separated on a 500 µm mesh.
Analyses
In the laboratory, all individuals were identified to the spe-
cies level using taxonomic keys available for the study area
(e.g., Retamal 2000; Zagal et al. 2007; Häussermann and
Försterra 2009; Reyes and Hüne 2012; Retamal and Ferrada
2016), and taxonomic expertise remained constant through
the entire sampling period; those specimens for which the
species could not be determined were identified to the genus
level. Species were then assigned to different feeding guilds
(Laudien et al. 2007). Individual specimens were meas-
ured (mm) and weighed using a precision analytic balance
(wet weight in grams, 0.001 g sensitivity). Carnivorous and
scavenger species accounted for over 95% of the observed
individuals in this community, and subsequent analyses
were, therefore, restricted to these well-represented feeding
strategies. In keeping with previous studies (Siemann et al.
1996, 1999), we assessed the individual-based relationships
between abundance (A), species richness (S), and body size
for each of the samples. Briefly, we summed the number
of species and the number of individuals across different
­loge weight classes. These weight classes were defined using
the progression class(i) = exp(i), with i = − 6, − 5, … 5, 6;
which yielded 13 equidistant body size classes on a logarith-
mic scale encompassing the observed range of individual
weights. Once these weight classes were defined, the total
number of species and the total number of individuals within
Power law : S = cTw
c w R2 BIC ∆i(BIC)
15.47 ± 0.77*** 0.22 ± 0.02*** 0.97 30.25 3.86
14.63 ± 0.49*** 0.25 ± 0.01** 0.87 194.05 8.72
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 15   Page 4 of 13
Fig. 1  Trivariate relationship between log body size, species richness,
and abundance in the benthic megafauna community of Coliumo Bay,
in January 2009, for species and individual level binned data (filled
and open circles, respectively). a Unimodal relationship between
body size and abundance. b Unimodal relationship between body size
each class were calculated, allowing species to potentially
occupy more than one size class. In addition, we repeated
that the analyses using species-based approach, where each
species’ body size was assigned to the mean value observed
on a given sampling date. The procedure outlined earlier
was then repeated to allow us to obtain the total number of
species and the total number of individuals within each class
were calculated, with species occupying a single size class.
Data tabulation was carried out using the tidyverse package
(Wickham 2017) available in the R program (R Develop-
ment Core Team 2019, available at www.r-proje​ct.org).
We used two complementary approaches to determine the
STR for each body size class. First, we calculated the accu-
mulated number of species at time t = i. To do so, we tallied
the total number of species observed from the first sample
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Marine Biology (2020) 167:15
and species richness. c Power-law scaling relationship between abun-
dance and species richness (continuous and segmented lines show the
fitted scaling relationship). d Tri-variate relationship between species
richness (z), abundance (y), and body size (x). See statistical explana-
tion in Supplementary Material II
to sample I; this procedure was done for the full data set, as
well as for each body size class. We refer to this as the tem-
poral species accumulation curve (TSAC). This procedure
is similar to species accumulation approaches for estimating
species richness based on incidence (Moreno and Halffter
2000; Ugland et al. 2003; Colwell et al. 2004). However,
here, we focused only on the observed sequence of samples
rather than on randomized curves, allowing us to follow the
exact temporal sequence of species increase observed over
time. In addition to the TSAC, we estimated the nested spe-
cies–time relationship (NSTR) using the sample accumu-
lation procedure described previously (Adler et al. 2005;
White 2007). Briefly, a time span window (T) is passed over
a time series of species lists, one for each time step, and all
species occurring within the window are counted (Adler and
Marine Biology (2020) 167:15 Page 5 of 13  15
Fig. 2  Time and body size effects on species richness. a Observed
species richness (open squares), temporal species accumulation curve
(filled circles), and the species–time relationship (open circles). The
fitted temporal trend in observed species richness is shown by the
dotted line, while the continuous and dashed lines show the power
functions fitted to the TSAC and NSTR, respectively. b Accumulated
species richness for species-level binned NSTR data over 1  month
(filled circles), 12  months (open circles), and 21  months (filled
squares). c Accumulated species richness for individual-level binned
NSTR data over 1  month (filled circles), 12  months (open circles),
and 21 months (filled squares)
Lauenroth 2003; Adler et al. 2005); this sliding window, or
nested, approach is equivalent to that used to construct fully
nested SARs (Plotkin et al. 2000). Observed species richness
values for each time span were then averaged to provide a
single estimate of mean species richness for that particular
time span, and the means were plotted as a function of time
span (Adler et al. 2005; White 2007). Again, this procedure
was done for the full data set as well as for each body size
class. All graphs were generated using packages ggplot2 and
plot3d available in the R software (Wickham 2016; Soetaert
2017; R Development Core Team 2019). It is clear that for
a fixed pool of species, be it at the community or metacom-
munity level, the number of species observed will tend to
increase as more individuals are sampled (Fisher et al. 1943;
Gotelli and Colwell 2001). Given that both the TSAC and
NSTR are constructed by accumulating successive samples,
it is clear that longer time spans also contain a greater num-
ber of individuals and, therefore, a greater number of spe-
cies. However, we also characterized the number of species
as a function of the number of individuals in each size class
as samples are accumulated in time. To that end, we fol-
lowed previous studies and fitted a power function to these
accumulated species-individual functions:
S = aI b , (5)
where a and b are the power-law parameters (Siemann et al.
1996, 1999; Fa and Fa 2002; McClain 2004). Power func-
tion and logarithmic function fits were carried out on log-
transformed data where appropriate, using ordinary linear
least squares regression (OLS) in the R program (R Devel-
opment Core Team 2019, available at www.r-proje​ct.org).
We compared the performance of logarithmic and power-
law relationships using the Bayesian Information Criterion
(BIC or Schwarz Criterion), selecting the lesser BIC as the
best model. For clarity, we also calculated the BIC deltas,
∆BICi = BICi-min (BIC), which provide a measure of the
strength of the evidence against the model with the higher
BIC value. The observed ∆BIC values were interpreted fol-
lowing Kass and Raftery (1995).
Results
Monitoring of the benthic megafauna community of Coli-
umo Bay, from January 2007 to January 2009, with trawl
sampling gear allowed us to capture, identify, measure,
and weigh 38,193 individuals. The data show this to be a
diverse community, with representation of four phyla, and
five classes (Asteroidea, Elasmobranchii, Actinopterygii,
Malacostraca and Gastropoda). Over the whole study period,
we observed a total of 33 species belonging to 12 orders and
26 families (Supplementary Material I, Table 1). In keep-
ing with the previous findings (Siemann et al. 1996, 1999;
Fa and Fa 2002; McClain 2004; Labra et al. 2015), data
binned at both the species and individual level show that
both abundance and species richness in the benthic mega-
fauna at Coliumo Bay show unimodal relationships with
log body size classes (in Fig. 1a, b). We also observed that
species richness and abundance across body size classes
are related by a power function relationship (Fig. 1c). We
found a parabolic relationship between the three variables,
13
 15   Page 6 of 13
Fig. 3  a Time and body size effects on observed species richness in
Coliumo for a species-level TSAC in body size classes. b Species-
level NSTR in body size classes. c Individual-level TSAC in body
size classes. d Individual-level NSTR in body size classes. Body
size classes correspond to − 2, − 1, 0, 1, and 2 bins (shown by filled
and open circles, open triangles, and filled and open squares, respec-
tively). All fitted power-law relationships are shown with solid lines.
as shown by the trivariate plot (Fig. 1d) (May 1988; Siemann
et al. 1996); therefore, species richness is closely related to
body size and abundance. Binning the data at the species
level results changes these patterns, with narrower unimodal
relationships, and a different species-individual scaling
exponent, which changes from 0.26 ± 0.04 (mean ± 1 se) for
data binned at the species level to 0.33 ± 0.04 (mean ± 1 se)
for data binned at the level of individual organisms. Spe-
cies richness fluctuated around 15 species (Fig.  2a),
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Marine Biology (2020) 167:15
e Body size effects on the power-law exponents for TSAC (open
circles) and NSTR (filled circles) in species-level data. f Body size
effects on the power-law exponents for the TSAC (open circles)
and the NSTR (filled circles) in individual-level data. The solid and
dashed lines show the observed power-law exponent values for the
full TSAC data set and the full NSTR data set, respectively, consider-
ing all individuals regardless of body size
without showing a significant trend (OLS linear regression,
F1,7 = 2.8, p = 0.1382), while the temporal species accumu-
lation curve showed a steady increase of species richness
over time, following a power function (Fig. 2a, Table 1).
Although the logarithmic and Arrhenius power func-
tions produced similar goodness of fit to the TSAC curve
(R2 = 0.94 and 0.97 for each of these two functions, respec-
tively), observed BIC values indicate that the data show
stronger support for the power function (Table 1). Similarly,
Marine Biology (2020) 167:15 Page 7 of 13  15

Table 2  Species accumulation curve (TSAC) in the benthic megafauna at Coliumo Bay

Body size bins Logarithmic: S = c + w log(T) Power law: S = cTw
c w R2 BIC c w R2 BIC ∆i(BIC)

Individual level
 − 6 1 ± 0 *** 0 ± 0ns – − Inf – – – – –
 − 5 1 ± 0*** 0 ± 0ns 0.43 − 346.93 – – – – –
 − 4 0.89 ± 0.25** 0.67 ± 0.10*** 0.84 7.41 1.07 ± 0.18*** 0.34 ± 0.06*** 0.87 6.80 0.66
 − 3 1.41 ± 0.65 ns 1.18 ± 0.26** 0.71 24.34 1.49 ± 0.35** 0.41 ± 0.09** 0.84 20.27 4.07
 − 2 4.24 ± 0.28*** 1.59 ± 0.11*** 0.96 9.01 4.66 ± 0.35*** 0.22 ± 0.03*** 0.93 15.73 6.72
 − 1 0.98 ± 1.64 ns 3.97 ± 0.66*** 0.81 41.15 2.37 ± 0.60** 0.58 ± 0.09*** 0.92 34.47 6.68
 0 6.88 ± 0.52*** 3.05 ± 0.21*** 0.96 20.48 7.65 ± 0.56*** 0.25 ± 0.03*** 0.95 24.90 4.42
 1 7.75 ± 0.43*** 3.11 ± 0.18*** 0.98 17.23 8.39 ± 0.42*** 0.24 ± 0.02*** 0.92 19.50 2.27
 2 5.05 ± 0.83*** 2.44 ± 0.33*** 0.87 28.77 5.30 ± 0.50*** 0.29 ± 0.03*** 0.94 23.50 5.28
 3 4.20 ± 2.10 ns 4.31 ± 0.85** 0.76 45.56 4.65 ± 0.97** 0.45 ± 0.07*** 0.90 39.32 6.24
 4 4.19 ± 0.76*** 2.19 ± 0.31*** 0.86 27.25 4.56 ± 0.52*** 0.29 ± 0.04*** 0.91 24.68 2.57
 5 2.50 ± 1.21 ns 3.02 ± 0.48*** 0.82 35.57 2.96 ± 0.44*** 0.47 ± 0.05*** 0.95 25.39 10.18
 6 0.39 ± 0.64 ns 2.01 ± 0.26*** 0.88 24.18 1.35 ± 0.35** 0.53 ± 0.09*** 0.91 23.21 0.96
Species level
 − 2 0.65 ± 0.48 ns 0.47 ± 0.18** 0.44 5.25 1.01 ± 0.31* 0.23 ± 0.11 ns 0.48 6.08 0.83
 − 1 2.62 ± 1.18 ns 2.56 ± 0.44** 0.82 19.53 0.78 ± 0.78 ns 0.62 ± 0.17* 0.76 23.24 3.71
 0 3.86 ± 0.31*** 1.42 ± 0.12*** 0.94 10.64 4.08 ± 0.23*** 0.23 ± 0.02*** 0.93 8.86 1.78
 1 1.27 ± 0.61 ns 2.83 ± 0.24*** 0.94 23.18 2.35 ± 0.26*** 0.48 ± 0.04** 0.97 16.79 6.39
 2 3.61 ± 0.46*** 1.67 ± 0.18*** 0.91 18.16 3.87 ± 0.31*** 0.27 ± 0.03*** 0.94 14.94 3.22
 3 − 1.61 ± 1.95 ns 3.36 ± 0.78** 0.69 44.20 0.40 ± 0.20 ns 1.04 ± 0.16*** 0.93 31.70 12.50
 4 1.88 ± 0.88 ns 1.89 ± 0.35** 0.77 29.88 2.18 ± 0.45** 0.43 ± 0.07*** 0.88 24.98 4.90
 5 0.11 ± 0.75 ns 1.60 ± 0.30** 0.77 27.10 0.62 ± 0.16** 0.71 ± 0.09*** 0.95 15.56 11.54
 6 − 0.11 ± 0.84 ns 1.64 ± 0.34** 0.74 29.05 0.47 ± 0.14* 0.79 ± 0.10*** 0.95 16.06 12.99

The table shows the fit of the logarithmic (S = c + w log (T)) and power-law (S = cTw) scaling models. For each of these relationships the table
shows the fitted values of the constant c and species richness scaling exponent w, with their corresponding standard errors. Also shown are the
R2, BIC, and ∆BIC values. Minimum values of BIC within each row are highlighted in bold, indicating the selected model. Bins − 6 to − 3 are
not shown, as no data were observed after estimating species average body sizes. Significance levels for the fitted parameters are shown using the
same abbreviations as Table 1. See text for details on the meaning of the different parameters

the NSTR for the complete data set also shows an increase
in species number (Fig. 2a), with comparable goodness of
fit for both functions, but with a broader scatter as shown
by observed R2 values of 0.87 for both methods. Again, the
BIC values indicate that the power function has stronger
support than the logarithmic function (Table 1). Having
determined the functional form of the TSAC and NSTR for
this data set, we then examined the effect of body size on
the number of species over increasing periods of time. We
find that species richness showed a unimodal dependence
on body size, a pattern which becomes more pronounced
as the length of the temporal window increases (Fig. 2b,
c), indicating that the rate of accumulation of species over
time depends on the body size of the individuals, as more
species are described for the central body size bins. This
pattern is observed for both levels of data aggregation, with
the pattern for data aggregated at the species level (Fig. 2b)
showing a narrower curve than data aggregated at the level
of individual (Fig. 2c). For species-binned data, temporal
species accumulation curve across the different body size
categories indicates that the rates of TSAC depend on body
size, being steeper for modal size classes (Fig. 3a, Table 2),
with a similar pattern observed for the species–time rela-
tionship (Fig. 3b, Table 3). For individual-binned data, both
TSAC and NSTR show a similar dependence on body size,
with more species accumulating faster in modal size classes
(Fig. 3c, d, Tables 2 and 3). Regarding the support for either
functional form of the TSAC and NSTR, we found that the
Arrhenius equation tended to provide a better model fit (as
shown by a lower BIC and higher R2) than the logarithmic
function (Tables 2 and 3). For both data-binning strategies,
fitted power-law exponents tended to be larger for both rela-
tionships than those values estimated for the full data set
(Fig. 3e, f, Tables 2 and 3). Hence, we see that both time
and body size do affect the number of species, regardless of
how body size is binned. The joint effect of body size and
time on observed species richness showed that the logarithm
of species richness can be well fitted by a three-dimensional

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 15   Page 8 of 13 Marine Biology (2020) 167:15

Table 3  Nested species–time relationships (NSTR) in the benthic megafauna at Coliumo Bay

Body size bins Logarithmic: S = c + w log(T) Power law: S = cTw
C w R2 BIC c w R2 BIC ∆i(BIC)

Individual level
 − 6 1 ± 0*** 0 ± 0ns*** 0.48 − 1936.22 – – – – –
 − 5 1 ± 0*** 0 ± 0ns 0.46 − 1683.21 – – – – –
 − 4 0.62 ± 0.31ns 0.45 ± 0.13** 0.23 72.98 0.55 ± 0.19** 0.45 ± 0.13*** 0.33 69.89 3.09
 − 3 1.01 ± 0.42* 1.23 ± 0.19*** 0.52 123.97 1.78 ± 0.23*** 0.50 ± 0.08*** 0.61 117.29 6.68
 − 2 2.81 ± 0.48*** 1.84 ± 0.24*** 0.57 180.71 3.05 ± 0.38*** 0.35 ± 0.05*** 0.61 177.99 2.72
 − 1 3.51 ± 0.49* 2.95 ± 0.24*** 0.77 181.92 3.92 ± 0.33*** 0.40 ± 0.03*** 0.82 171.69 10.22
 0 6.52 ± 0.46*** 2.93 ± 0.23*** 0.79 176.37 6.86 ± 0.38*** 0.28 ± 0.02*** 0.82 172.12 4.25
 1 7.58 ± 0.30*** 2.92 ± 0.15*** 0.90 137.93 7.92 ± 0.25*** 0.25 ± 0.13*** 0.91 133.18 4.75
 2 5.57 ± 0.70*** 2.53 ± 0.18*** 0.83 152.79 5.97 ± 0.31*** 0.27 ± 0.02*** 0.83 153.58 0.79
 3 5.05 ± 0.58*** 4.00 ± 0.28*** 0.82 196.52 5.66 ± 0.40*** 0.39 ± 0.03*** 0.86 185.92 10.60
 4 3.89 ± 0.37*** 2.07 ± 0.18*** 0.75 155.41 4.15 ± 0.29*** 0.31 ± 0.03*** 0.78 151.67 3.74
 5 2.71 ± 0.56*** 3.00 ± 0.27*** 0.73 193.88 3.30 ± 0.38*** 0.45 ± 0.05*** 0.77 187.61 6.27
 6 1.98 ± 0.29*** 1.56 ± 0.14*** 0.73 134.41 2.28 ± 0.22*** 0.38 ± 0.04*** 0.75 132.38 2.03
Species level
 − 2 0.91 ± 0.26*** 0.27 ± 0.09*** 0.20 44.47 0.94 ± 0.19*** 0.21 ± 0.08* 0.24 44.11 0.36
 − 1 1.00 ± 0.40* 1.23 ± 0.19*** 0.50 140.49 1.28 ± 0.25*** 0.46 ± 0.08* 0.55 136.77 3.71
 0 2.02 ± 0.48*** 1.58 ± 0.22*** 0.54 159.43 2.09 ± 0.32*** 0.42 ± 0.06* 0.62 152.26 7.17
 1 2.28 ± 0.30*** 2.12 ± 0.15*** 0.83 137.42 2.53 ± 0.17*** 0.44 ± 0.03** 0.90 113.50 23.92
 2 2.69 ± 0.34*** 1.84 ± 0.16*** 0.75 140.42 2.98 ± 0.25*** 0.37 ± 0.03*** 0.78 135.22 5.2
 3 1.17 ± 0.64ns 2.68 ± 0.31** 0.64 188.46 1.80 ± 0.32*** 0.58 ± 0.07*** 0.73 177.06 11.40
 4 1.68 ± 0.30*** 1.71 ± 0.15*** 0.75 138.97 1.95 ± 0.20*** 0.45 ± 0.04*** 0.80 129.26 9.71
 5 0.70 ± 0.24** 1.39 ± 0.11*** 0.78 104.17 0.99 ± 0.10*** 0.57 ± 0.40*** 0.88 77.34 26.83
 6 0.87 ± 0.32* 1.42 ± 0.15*** 0.66 129.74 1.16 ± 0.18*** 0.53 ± 0.06*** 0.74 119.29 10.45

The table shows the fit of the logarithmic (S = c + w log (T)) and power-law (S = cTw) scaling models. For each of these relationships the table
shows the fitted values of the constant c and species richness scaling exponent w, with their corresponding standard errors. Also shown are the
R2, BIC, and ∆BIC values. Minimum values of BIC within each row are highlighted in bold, indicating the selected model. Significance levels
for the fitted parameters are shown using the same abbreviations, as shown in Table 1. See text for details on the meaning of the different param-
eters

parabolic function, reflecting the unimodal pattern with body
size as well as the steady increase in species richness. For
species-level aggregated body size, data showed a signifi-
cant effect on ­log10(species richness), with TSAC and NSTR
showing R2 values of 0.69 and 0.64, respectively (Fig. 4a,
b). Similarly, in individual-level aggregated body size data,
a significant effect of body size and time was observed, with
TSAC and NSTR curves showing R2 values of 0.90 and
0.0.82, respectively (Fig. 4c, d). Hence, while species bin-
ning reduces the range of observed body size classes present
(Fig. 1), the effect of body size on the overall pattern of tem-
poral accumulation of species is still observed. Finally, it is
interesting to consider the effect of the accumulation process
on the relationship between species richness and abundance.
When we examine this scaling relationship, we find that sig-
nificant power-law scaling relationships are found for both
data binning strategies (Fig. 5a, b), with the TSAC showing
better goodness of fit than the NSTR in both the species-
level data ( R2TSAC = 0.59 vs. R2STR = 0.29) and the individual
level aggregated data ( R2TSAC = 0.82 vs. R2STR = 0.69). These
patterns show a significant effect of time, with a clearer pat-
tern emerging for data aggregated at the level of species
(Fig. 5c, d), than for data aggregated at the level of individu-
als (Fig. 5e, f).
Discussion
In this study, we examined the empirical relationships
between the number of species and sampling time, body
size, and abundance in a shallow marine benthic megafauna
(or megabenthic) community. We explicitly consider the
effect of the data aggregation strategy, comparing results
obtained when species-based relationships vs. individual-
based ones. Our results show that the number of species
at Coliumo Bay depends on both the sampling time inter-
val as well as the number of individuals across body size

13
Marine Biology (2020) 167:15 Page 9 of 13  15
Fig. 4  a Effects of time and body size on species richness. Effects
of increasing time span and body size classes are shown for a
species-level TSAC fitted with a 3-D non-linear regression func-
tion ­log10(S) = 0.36 + 0.13·T + 0.02·W − 0.03·W2 (R2 = 0.69). b
Species-level NSTR fitted with a 3-D non-linear regression func-
tion ­log10(S) = 0.33 + 0.14·T + 0.03·W − 0.03·W2 (R2 = 0.64). c
classes. Both abundance and species richness across log
body size classes followed a unimodal relationship in the
samples examined, providing support for the generality
of unimodal individual size spectra, as found in grassland
insects and gastropods (Siemann et al. 1996, 1999; Fa and
Fa 2002; McClain 2004; Labra et al. 2015). Interestingly,
although community composition and dominant species
size structure in Coliumo Bay experienced major changes
during the study period (Hernández-Miranda et al. 2010,
2012a, b), the scaling pattern of species increase with time
is clear. Furthermore, the rate of species increase is also
Individual-level TSAC fitted with a 3-D non-linear regression func-
tion ­log10(S) = 0.85 + 0.07·T + 0.02·W − 0.02·W2 (0.90). d Individ-
ual-level NSTR fitted with a 3-D non-linear regression function
­log10(S) = 0.78 + 0.08·T + 0.02·W − 0.02·W2 (R2 = 0.82). All regression
parameters were significant, with p < 0.001 (see also Supplementary
Material I, Table 2)
clearly dependent on body size. Previous results have shown
that a unimodal relationship between species richness, body
size, and abundance is a general feature of the epibenthic
faunal community at Coliumo Bay (Labra et al. 2015). Our
results show that this unimodal relationship also has effects
on the rate of increase in species richness with time, and
holds true for both species-based analyses and individual-
based analyses. Moreover, although a good deal of vari-
ability can be ascribed to differences between body size
classes, we found that both the species accumulation curve
(TSAC) and the nested species–time relationship (NSTR)
13
 15   Page 10 of 13 Marine Biology (2020) 167:15

13
 Marine Biology (2020) 167:15 Page 11 of 13  15
◂Fig. 5  Relationship between species richness, abundance, and time
within body size classes. Bivariate relationship between species rich-
ness and abundance across species-level body size classes data (a)
and individual-level body size classes data (b). Open and filled cir-
cles showing data for the TSAC and the NSTR curves. In a and b, the
continuous line shows the fitted function for TSAC, while the dashed
line shows the fitted function for the NSTR relationships. Effects of
increasing time span and body size classes on TSAC (c) and NSTR
(d) calculated for species-level binned body size classes, fitted with
a 3-D linear function. Effects of increasing time span and body size
classes on TSAC (e) and NSTR (f) calculated for individual-level
data, fitted with a 3-D linear function. See statistical explanation in
Supplementary Material II
were better fit by the Arrhenius power-law model than by
the logarithmic model. Therefore, despite the typical sea-
sonal and inter-annual variability in species composition and
community structure, the benthic megafauna community at
Coliumo Bay presents general macro-ecological patterns in
the accumulation of species. This is particularly interesting
in light of the known disturbances experienced by this area
(Hernández-Miranda et al. 2010, 2012a, b). In January 2008,
Coliumo Bay experienced a strong hypoxic disturbance
that resulted in massive mortality and stranding of fish and
marine invertebrates at Coliumo Bay (Hernández-Miranda
et al. 2010, 2012b, 2017). Following this hypoxic distur-
bance total community abundance increased, mostly due to
the recruitment of gastropod scavenger snails Nassarius spp.
which were favored by the hypoxic mass mortality event
(Hernández-Miranda et al. 2012a, b). The January 2008
sample was taken 4 days after this event, but remarkably, the
abrupt changes in community composition or structure are
not reflected in the patterns shown here. This suggests that
while this local marine megabenthic community may have
been strongly impacted by the hypoxia, regional processes
may have allowed the continued immigration of individuals
and the steady increase in observed species richness. The
ecological mechanisms of Response Diversity and Cross
Scale Resilience were proposed by Hernández-Miranda
et al. (2012a) as responsible for this sudden recovery of the
epibenthic faunal community after the strong perturbation.
Another interesting point is the fact that previous analyses
of the species–time relationship have focused mostly on ter-
restrial taxonomic assemblages, with the sole exceptions of
corals, algae, and intertidal invertebrates as the only marine
examples (Adler et al. 2005; White 2007). The results of
this study provide further evidence for the generality of the
species–time relationship. The observed rates of increase in
species richness over small to medium species likely respond
to seasonal effects on reproductive patterns, with greater
frequencies of smaller individuals during spring resulting
from the arrival of new individuals or recruits. Reproduc-
tion patterns in neritic and benthic communities inhabiting
coastal areas off Central Chile in the Humboldt Current Sys-
tem have been shown to follow a marked seasonal pattern,
with the reproductive period occurring at the end of winter
and/or the beginning of spring, leading to recruitment events
during spring (Hernández-Miranda et al. 2003, 2010). On
the other hand, the greater rate of increase in larger species
reflects the influx of larger, more mobile organisms such
as rays or the banded toadfish Aphos porosus (Hernández-
Miranda et al. 2012b).
By and large, the search for general causal relation-
ships has left ecology with very few patterns that may be
accepted as laws (Lawton 1999); the SAR and STR are
among the few general patterns that may be considered as
such (Rosenzweig 1995; Lawton 1999; Adler and Lauen-
roth 2003; Adler et al. 2005). In addition, macroecologists
have mostly focused on univariate or bivariate relation-
ships (e.g., Gaston and Blackburn 2000; Blackburn and
Gaston 2004) when examining statistical relationships
among variables such as body size, abundance, geographic
range, size, and species richness, though some authors
have examined trivariate relationships (Siemann et  al.
1996, 1999; Fa and Fa 2002; McClain 2004). In this study,
we have shown how body size is important in determin-
ing the number of species observed over a given period of
time, even when considering the effect of a major hypoxic
natural perturbation. While several authors have focused
on the potential role of body size and environmental varia-
bles in accounting for observed biodiversity patterns (e.g.,
Storch et al. 2007; Harte 2011; Sibly et al. 2012), not many
authors have focused on the study of trivariate relation-
ships such as those reported by Siemann et al. (1996), or
on the impact of the trivariate relationship on other pat-
terns such as the TSAC or NSTR. While our results show
that the accumulation of species richness in time is related
to the trivariate relation between richness, abundance, and
body size, and the observed pattern does not necessarily
make clear which mechanisms may underlie it. As indi-
cated by Adler and Lauenroth (2003), ecological patterns,
such as the increase in species richness with time and
area, are not the result of environmental variability, but
rather emerge from the interaction between environmental
variability and biological processes operating at the scale
of individual organisms, populations, and communities
(Adler and Lauenroth 2003; Adler et al. 2005; White et al.
2006). As we have discussed above, observed community
dynamics are strongly influenced by the responses to envi-
ronmental disturbance (Hernández-Miranda et al. 2010,
2012a, b). Our results show that the species-based pattern
shows a narrower range of body sizes than that observed
for the individual-based analysis. A relevant point to bear
in mind is that the generality of the trivariate relationship
between richness, abundance, and body size suggests that
some common mechanism could be acting in ecosystems
as diverse and distinct as grasslands and benthic marine
communities (Siemann et al. 1996, 1999; Fa and Fa 2002;
13
 15   Page 12 of 13
McClain 2004). Given the time and spatial scale at which
these studies have been carried out, we suggest that the
observed patterns reflect the outcome of contemporary
demographic processes subject to the constraints of pat-
terns of body size distribution across species. Hence, the
species-level pattern reflects the constraints in life history
and body size distribution across taxa, while individual-
based analyses reflect the result of recent demographic
processes. An interesting point is that although individual-
based data are certainly not independent from a compara-
tive perspective, the observed abundance and richness
across body size classes do reveal information on the result
of demographic transitions of individuals from all spe-
cies. These include the effect of processes such as recruit-
ment, growth and migration, particularly of juveniles (in
the smaller body size classes) as well as movement of
larger individuals (in the larger body size classes). Nev-
ertheless, our results do not allow us to ascertain which
particular combination of these factors may be at play at
Coliumo at any given time. Future work should not only
examine the generality of these relationships in other taxa
and ecological systems, but aim to design methodological
and analytical frameworks that allow a better assessment
of the relative importance of contemporary demographic
processes vs. historical constraints on morphological and
life history trait distributions.
Acknowledgements  The author thanks EHM’s laboratory members for
their assistance during field and laboratory activities. In addition, the
authors would like to thank three reviewers for their valuable comments
and suggestions to improve the quality of the manuscript.
Author contributions  FAL, EHM, and RQ conceived the idea; FAL
and EHM assembled the database; FAL analyzed the data; FAL, EHM,
and RQ wrote the paper. All authors contributed to the drafts and gave
final approval for publication.
Compliance with ethical standards  and pitfalls in the measurement and comparison of species rich-
Conflict of interest  All authors declare that they have no conflict of
interest and that all applicable guidelines for sampling of organisms
have been followed. This study was funded by the Programa de In-
vestigación Marina de Excelencia (PIMEX), of the Faculty of Natu-
ral and Oceanographic Sciences (University of Concepción, Chile).
R. Quiñones and E. Hernández-Miranda received additional funding
from INCAR (FONDAP Nº15110027). F. A. Labra received fund-
ing from PIA-CONICYT ACT-172037 Grant. E. Hernández-Miranda
also received additional funding from FONDECYT 11100334, and
1130868 Grants.
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