Download Convergence in Morphological Patterns and Community

vol. 158, no. 5
the american naturalist
november 2001
Convergence in Morphological Patterns and Community
Organization between Old and
New World Rodent Guilds
Ariela Ben-Moshe,1 Tamar Dayan,1,* and Daniel Simberloff 2,†
1. Department of Zoology, Tel Aviv University, Ramat Aviv, Tel
Aviv 69978, Israel;
2. Department of Ecology and Evolutionary Biology, University of
Tennessee, Knoxville, Tennessee 37996-1610
Submitted August 22, 2000; Accepted May 23, 2001
abstract: We studied morphological relationships within three
guilds of gerbillid rodents in Israel. We found a nonrandom pattern
of overdispersed means (community-wide character displacement)
for upper incisor widths among the species in these three guilds.
Upper tooth-row lengths, condylo-basal skull lengths, and tooth-row
surfaces displayed similar patterns. We also studied seed-size selection
by two well-studied gerbil species, which have previously been found
to compete, in order to test whether specializing on husking seeds
of different sizes as a mechanism of coexistence may underlie the
morphological patterns. The seed-size selection experiments took
place in two large aviaries with artificial lighting simulating full-moon
nights, which is when predation risk is perceived as high. Seeds of
different sizes (commercial seeds in one experiment and husked
wheat particles in the other) mixed with sand were offered in trays.
The larger Gerbillus pyramidum took significantly larger commercial
seeds and marginally larger wheat particles than the smaller Gerbillus
allenbyi. The patterns attest to ecomorphological convergence at the
guild level; we previously demonstrated size structuring in several
North American heteromyid rodent guilds, and we now report similar size structuring among Israeli gerbillid guilds. The occurrence
of convergent community structure strongly indicates general rules
governing ecological communities or guilds.
Keywords: community-wide character displacement, community
structure, ecomorphology, guild convergence, seed-size selection.
A major goal of ecology is identifying and interpreting
recurring patterns in ecological communities. Elucidating
* Corresponding author; e-mail: [email protected].
†
E-mail: [email protected].
Am. Nat. 2001. Vol. 158, pp. 484–495. 䉷 2001 by The University of Chicago.
0003-0147/2001/15805-0003$03.00. All rights reserved.
such patterns affords the possibility to understand the
forces that structure ecological communities, to fathom
the rules that govern them, in fact, to determine whether
such rules exist at all (cf. Lawton 1999), and, if they do,
to assess their generality.
The occurrence of convergent community structure
would strongly indicate general governing rules. If similar
selection regimes produce similarly structured ecological
communities, then general structuring rules can be sought
and analyzed. Since whole ecological communities are extremely complex entities, ecologists usually study parts of
communities. Ecological guilds (sensu Root 1967) have
often been taken as such manageable units that allow detailed study (Simberloff and Dayan 1991); therefore, the
search for guild convergence may be more promising than
the search for convergence between entire communities.
If guilds are building blocks of communities, understanding their structure and the forces operating within them
may provide insight into the structure and function of
communities.
A conspicuous case of apparent convergence is found
among two of the most thoroughly studied mammalian
ecological guilds: the North American desert rodents of
the family Heteromyidae and members of the Old World
family Gerbillidae (Abramsky 1983). Most convergences
and parallels are recognized by striking visual resemblances
(Begon et al. 1990); general similarities in size and color,
inflated tympanic bullae, and a tendency toward bipedal
locomotion (albeit to different degrees) occur in both families. Seeds of ephemeral desert plants are a major item in
the diet of heteromyids and gerbillids, and this similarity
in resource base plus the general morphological similarities
among these two groups of taxonomically distantly related
rodents are often taken as a case of evolutionary convergence (Brown et al. 1979; Abramsky et al. 1985). However,
Brown et al. (1994) propose that this apparent morphological convergence may be superficial; they base this conjecture on dietary differences between potential analogous
members of heteromyid and gerbillid guilds rather than
Old and New World Rodent Guilds 485
on specific measures of morphology. In fact, they see an
intriguing lack of morphological convergence between granivorous rodents of the Old World and New World and
suggest that factors that shape the more conspicuous attributes of species may not be the same as those that
promote or inhibit species coexistence.
One manifestation of community or guild morphological structure is community-wide character displacement
(sensu Strong et al. 1979), which is the occurrence of
nonrandom size relationships among guild members
(means for the different species overdispersed). This phenomenon has generally been interpreted as resulting from
interspecific competition and resource partitioning by
food size as a mechanism of coexistence (e.g., Holmes and
Pitelka 1968; Dayan et al. 1989a, 1989b, 1990, 1992; Dayan
and Simberloff 1994a). Such size-structured communities
or guilds may arise from species sorting and/or from an
actual coevolutionary change and may attest to the ecological and evolutionary importance of competition in
structuring ecological communities (Case and Sidell 1983;
Case et al. 1983; Sinclair et al. 1985a, 1985b; Dayan and
Simberloff 1998).
Community-wide character displacement has been described for sets of species in both Old and New World
seed-eating rodent guilds (Yom-Tov 1991 and Dayan and
Simberloff 1994b, respectively). Were such morphological
patterns convergent, they could indicate shared, underlying community-wide selective forces. Curiously, however, the patterns have been found in different morphological characters and have been given different
interpretations.
Dayan and Simberloff (1994b) demonstrated regular
morphological relationships among the upper incisors of
heteromyid rodents. Incisors of heteromyids are used for
husking, some of which takes place aboveground where
predation risk is high (Rosenzweig and Sterner 1970; Lemen 1978). Therefore, husking speed may be critical (Rosenzweig and Sterner 1970). Dayan and Simberloff (1994b)
hypothesized that for each species there may be an optimal
seed size, too large to be efficiently stored in the heteromyids’ external cheek pouches without husking but that
can be husked efficiently enough to outweigh the risk of
predation, which merits being the target of specialization.
The strong relationship between pouch volume and incisor
width for these species supports this hypothesis. Specializing on different seed sizes may result from competition
between coexisting heteromyids (Dayan and Simberloff
1994b).
For tooth-row lengths and surfaces, Dayan and Simberloff (1994b) found no regular pattern for heteromyids
and suggested that, since grinding takes place in the safety
of the burrow where there is no time constraint, selection
pressure on this trait should not be strong. On the other
hand, Yom-Tov (1991), who studied morphological relationships among the gerbillines of Israel, measured two
characters, skull length and upper tooth-row length, and
demonstrated overdispersed means for the latter trait. He
suggested that the longer the tooth row, the more grinding
area is available for each jaw movement; species with
longer tooth rows may feed on harder and larger seeds
and on a higher proportion of leaves and stems, which
are often hard and include silica (Yom-Tov 1991).
How do we reconcile these differing patterns and hypotheses for tooth morphology between the gerbillines and
heteromyids? Do they indicate different guild-level selective forces in the two groups? The apparent convergence
noted by Abramsky (1983) may simply reflect a striking
overall visual resemblance, while ecological detail as reflected by teeth defies this interpretation (see pp. 23–25
in Begon et al. 1990).
We carried out a comparative morphological study of
Israeli gerbillines plus cafeteria studies of seed-size selection, with the following specific goals: to test for convergent morphological patterns between Israeli and North
American seed-eating rodents and to determine whether
seed-size selection facilitates coexistence among Israeli gerbillids, as it appears to do for North American heteromyids. We sought insight into the possible relationship
between convergence in morphological patterns and convergence in forces organizing communities in Old and
New World granivorous desert rodents.
Material and Methods
Seed-Eating Rodent Guild
Yom-Tov (1991) studied the gerbilline rodents of Israel,
which he viewed as a single group, and we follow his guild
assignation. The jerboa (Jaculus jaculus) also constitutes
part of the same rodent community (Brown et al. 1994),
but neither Yom-Tov (1991) nor we include it in the gerbilline guild, owing to its different limb morphology
(hence, locomotor behavior; reviewed by Dayan and Simberloff 1998) and to its herbivorous diet (Osborn and
Helmy 1980; Bar et al. 1984). Yom-Tov (1991) included
the fat sand rat (Psammomys obesus) in the gerbilline rodent guild, and we do so tentatively. The fat sand rat
subsists mainly on Atriplex halimus (Daly and Daly 1973),
but no research has focused on its precise diet. Seeds have
been found in fat sand rat burrows (Anderson and de
Winton 1902 cited in Harrison and Bates 1991; M. Kam,
personal observation), and in captivity, fat sand rats can
subsist on a mixed diet of seeds and A. halimus (M. Avishai,
personal observation). However, because the evidence is
far from conclusive, we analyzed the rodent guild both
including and excluding this species.
486
The American Naturalist
We follow Yom-Tov (1991) in choice of geographical
regions and species studied: sand dunes of the southern
coastal areas (with four psammophile species: Meriones
sacramenti, Meriones tristrami, Gerbillus pyramidum, and
Gerbillus allenbyi), sand dunes of the northern Negev Desert (with seven psammophile species: P. obesus, M. sacramenti, Meriones crassus, G. pyramidum, G. allenbyi, Gerbillus gerbillus, and Gerbillus henleyi), and the sand dunes
of the Arava Valley (with four psammophile species: P.
obesus, M. crassus, G. gerbillus, and G. henleyi). Patterns
of local coexistence of these species have not been studied,
and our study is concerned with patterns where overlap
is at a geographical scale (see Dayan and Simberloff
1994b).
Morphological Study
We measured rodent skulls in the Tel Aviv University Zoological Museum. We took measurements with digital calipers (Mahr) to 0.01 mm precision for four characters:
condylo-basal length of the skull (CBL); upper incisor
width (IW), which estimates the width of the cutting edge
(Dayan and Simberloff 1994b); upper tooth-row length
(UTL), the length of the grinding surface; and width of
the upper tooth row—multiplying UTL by this measure
provides an estimate of molar tooth-row surface, or grinding surface (UTRS). These measures were also taken in
our heteromyid rodent study (Dayan and Simberloff
1994b), with the working hypothesis that seed-size selection would be best reflected by incisor width, whereas the
tooth-row length and, even more so, surface would reflect
the volume of food ingested, associated with body size and
metabolic needs (Gould 1975), as well as the amount of
plant material ingested (Yom-Tov 1991).
We measured specimens of the relevant species in the
Tel Aviv University Zoological Museum. Tooth wear was
noted for every specimen measured, and the degree of
tooth wear, measured by an index developed by Rahmut
Ben-Moshe (1996), was correlated with all four measures.
We found increasing growth during tooth-wear stages 1
and 2 that ceased at tooth-wear stage 3; therefore, in this
study, we analyzed only specimens from stage 3 growth
wear and older. Sample sizes (stage 3 and older) were 26
G. allenbyi, 13 G. pyramidum, six G. gerbillus, two G. henleyi, 46 M. tristrami, 22 M. sacramenti, 20 M. crassus, and
27 P. obesus.
Gerbils exhibit very low sexual-size dimorphism, with
a maximum of 4% difference in size between the sexes
(Rahmut Ben-Moshe 1996); therefore, we used mixed-sex
populations in our current study, as did Yom-Tov (1991)
for the same species and Dayan and Simberloff (1994b)
for heteromyid rodents.
To assess whether size ratios were more equal than ex-
pected by chance within a ranked sequence, we used Barton-David (B-D) statistics (Barton and David 1956; Simberloff and Boecklen 1981). For a line uniform-randomly
broken into segments, Barton and David calculated the
cumulative frequency distributions for the ratios of the ith
smallest segment to the jth smallest segment for all (i,j)
such that i ! j. If morphological sizes are based on a logarithmic line, lengths of segments correspond to size ratios,
and so the B-D statistics test whether pairs of size ratios
are more similar than would be expected if the species’
sizes were independently distributed according to a loguniform distribution. Boecklen and NeSmith (1985)
showed that points distributed log-normally give very similar B-D statistics. Throughout, we use three B-D statistics:
G1, n, the ratio of the smallest to the largest size ratio;
G1, n⫺1, the ratio of the smallest to the second largest size
ratio; and G 2, n, the ratio of the second smallest to the
largest size ratio. For detailed discussion of statistical tests
of size ratios, see Dayan and Simberloff (1998).
To test for morphological differences between mean
measurements in different geographic regions, we carried
out paired t-tests for each species because no species occurred in more than two regions. Because slight morphological differences may exist even where differences do not
appear significant, we carried out our B-D analyses on
both pooled assemblages (using means for specimens from
all geographic regions) and regional ones (means for specimens only from specific region included).
After we obtained results of the B-D tests, we sought
the probabilities of achieving these significance values in
three different regions by chance. Because the sets of species in the different regions overlap, there is no apparent
way to calculate a formal total probability. As noted above,
patterns of local coexistence for these rodents are unknown; therefore, we cannot emulate the methods of Bowers and Brown (1982). Following a technique of Losos et
al. (1989), we used Fisher’s test of combined probabilities
(Sokal and Rohlf 1981) on the G1, n statistics (the most
extreme comparison of size ratios), combining probabilities from all three regions. However, if the same size ratio
was used more than once in a test, the estimate of combined probability would be too low; that is, the test would
not be conservative and significance could be inflated.
Thus, we checked to see if ratios between the same two
species were being included more than once in each
calculation.
Seed-Size Selection
Studies of seed-size selection were carried out using only
two of the gerbilline species: G. allenbyi (24 g) and G.
pyramidum (39 g), which have been found to compete
(Abramsky et al. 1985, 1990, 1991). A problem in labo-
Old and New World Rodent Guilds 487
Table 1: Lengths (mm) of seeds used
in cafeteria experiments
Species
Mean
SD
Helianthus annuus
Avena sativa
Avena strigosa
Phalaris canariensis
Setaria italica
24.04
11.12
10.33
4.99
1.61
2.87
1.12
.93
.31
.05
to using these seeds in our experiment was that the seeds
were not husked; seeds found in nature are unhusked.
Therefore, our assumption was that gerbils confronted
with different sizes of palatable seeds would make similar
choices to those made under natural conditions.
Note: Means and standard deviations are
for 10 individuals of each species.
ratory experiments is that the rodents may not perceive
the same risks as do free-ranging gerbils, and this perception affects their natural foraging patterns (Abramsky et
al. 1991; Ziv 1991). Therefore, we carried out our experiments in a large, 5-m-high aviary (18 # 23-m enclosure
divided into two equal parts by a 1-m-high fence) at the
Blaustein Institute for Desert Research. We used artificial
lighting to simulate full-moon nights, which is when predation risk for these rodents is perceived as high (Kotler
et al. 1991). The seeds provided (2 Ⳳ 0.02 g of each
seed type [weighed by digital scales to 0.01 g precision])
were mixed with 5 L of sieved sand in trays measuring
45 # 60 # 2.5 cm in order to simulate natural foraging
conditions and costs. We carried out two experiments with
two types of seed.
Commercial Seeds. We used seeds of sunflower (Helianthus
annuus), cultivated oats (Avena sativa), wild oats (Avena
strigosa), canary grass (Phalaris canariensis), and foxtail
millet (Setaria italica). Sizes of these seeds are listed in
table 1. These specific seeds were chosen because of their
different sizes, following a preliminary cafeteria experiment to determine that the seeds were all palatable to
gerbils, and taken in significant quantities. The advantage
Different-Sized Particles of Husked Wheat. The wheat (cf.
Abramsky 1983; Price 1983; Price and Brown 1983) was
ground and then electrically sieved to three size groups:
14,000 m; 2,000–4,000 m; and 1,000–2,000 m. This range
of seed sizes is smaller than that of the commercial seeds
described above, and most of these particles are smaller
than most of the commercial seeds. The advantage of using
husked wheat is that the particles differ only in size. A
disadvantage is that we had essentially a continuum of
seed particle sizes rather than discrete size groups, as when
using commercial seeds of different sizes. Since these seed
particles required no husking and can be eaten immediately, our working hypothesis was that seed-size selection
would be of less importance in this case because the seeds
require no handling.
Seed trays were placed in the aviary at sunset and were
collected at sunrise. The seeds were sifted and weighed by
seed type. During an acclimatization period of at least a
week (to become familiar with the aviaries and trays), and
between experiments, the gerbils were fed with large, commercial mouse pellets. Before each experiment, we accustomed the gerbils to foraging in seed trays by feeding them
with mouse pellets mixed in the sand.
Because seeds may absorb humidity, we also placed a
control tray outside, to which gerbils had no access. In
the morning, we weighed the seeds in the control trays
and performed the following calculation: we divided the
original mass of the seeds by the mass of the seeds in the
morning and multiplied the seed weight that remained in
Table 2: Sample means and standard deviations (in parentheses) for the different measurements
of the different species
Species
Gerbillus allenbyi
Gerbillus gerbillus
Gerbillus henleyi
Gerbillus pyramidum
Meriones crassus
Meriones sacramenti
Meriones tristrami
Psammomys obesus
UTRS
CBL
5.57 (.34)
5.33 (.08)
2.73 (.04)
7.7 (.55)
10.27 (.92)
13.58 (.71)
8.99 (.92)
15.01 (1.68)
25.31 (.81)
25.08a (.19)a, 24.5b (.03)b
19.83 (.11)
28.87 (.83)
35.61 (1.64)
39.25 (1.90)
32.86 (2.29)
39.23a (4.20)a, 42.51b (1.88)b
IW
.81
.68
.49
.91
1.00
1.38
1.02
1.48
(.05)
(.04)
(.00)
(.05)
(.04)
(.15)
(.09)
(.15)
UTL
3.94
3.89
2.89
4.61
5.57
6.48
5.40
7.05
(.12)
(.08)
(.02)
(.17)
(.26)
(.24)
(.36)
(.45)
Note: The data are for specimens pooled from all regions. In the few cases where significant differences (by
paired t-tests; P ! .05) were found between specimens in different regions, we present the sample statistics for
the specific region. UTRS p molar tooth-row surface; CBL p condylo-basal length of the skull; IW p upper
incisor width; UTL p upper tooth-row length.
a
Negev region.
b
Arava region.
488
The American Naturalist
Table 3: Barton-David test results for the different characters measured in three different
regions
Trait
Negev:
UTL
IW
CBL
UTRS
Arava:
UTL
IW
CBL
UTRS
Coastal plain:
UTL
IW
CBL
UTRS
G1, 6
G1, 3
P
G1, 5
G1, 2
P
G2, 6
G2, 3
P
.0430
.2135
.0022
.0658
…
…
…
…
.566
.073
.971
.424
.0675
.2172
.0024
.1360
…
…
…
…
.596
.186
.981
.352
.2837
.2878
.0389
.1496
…
…
…
…
.171
.165
.912
.473
…
…
…
…
.6564
.8359
.4736
.5672
.038
.007
.115
.068
…
…
…
…
.7930
.8497
.8375
.5786
.148
.106
.115
.327
…
…
…
…
.8278
.9837
.5655
.9803
.153
.014
.425
.017
…
…
…
…
.8614
.3775
.7285
.3753
.005
.186
.022
.188
…
…
…
…
.9929
.9803
.9837
.4784
.005
.013
.011
.421
…
…
…
…
.8675
.3851
.7406
.7845
.116
.637
.238
.195
Note: The tests were calculated using means for specimens pooled from all three regions and including
all species. Significant or marginally significant (up to P p .075 ) results are in bold. For abbreviations,
see table 2.
the experimental trays by the resultant number, thereby
accounting for humidity-induced changes in seed mass.
We carried out two replicate experiments per species.
We trapped individuals of both species in the field and
placed five individuals of G. allenbyi in one part of the
aviary and five individuals of G. pyramidum in the other
part. Later, the gerbils were removed and new groups were
placed for the second experiment. No individual was used
in more than one replicate.
The two gerbil species differ in body mass, and individuals of the larger species are expected to consume
greater quantities of seed. Therefore, we calculated the
proportion of each seed type taken per night as part of
the total mass of seed taken that night and arcsine transformed the results. We carried out two-way ANOVAs (using STATVIEW; SAS 2000) to test for differences between
the species in seed choice and differences between replicate
experiments.
Results
Paired t-tests revealed that, except for two cases, CBLs of
Gerbillus gerbillus and Psammomys obesus (Negev Desert
and Arava Valley), there were no significant morphological
Table 4: Barton-David test results for the different characters measured in three different regions
Trait
Negev:
UTL
IW
CBL
UTRS
Arava:
UTL
IW
CBL
UTRS
Coastal plain:
UTL
IW
CBL
UTRS
G1, 6
G1, 3
P
G1, 5
G1, 2
P
G2, 6
G2, 3
P
.07255
.2219
.06122
.04392
…
…
…
…
.390
.066
.449
.559
.10641
.26957
.06947
.07341
…
…
…
…
.442
.122
.587
.569
.27785
.23378
.15666
.14894
…
…
…
…
.179
.254
.451
.476
…
…
…
…
.85731
.61851
.55750
.71320
.005
.050
.072
.025
…
…
…
…
.97937
.77348
.93274
.76902
.014
.163
.046
.167
…
…
…
…
.87536
.79964
.59771
.92741
.109
.180
.389
.062
…
…
…
…
.79294
.29333
.66753
.38605
.012
.275
.035
.178
…
…
…
…
.98729
.64471
.87986
.57764
.0085
.269
.083
.328
…
…
…
…
.80314
.45498
.75867
.66833
.176
.553
.220
.313
Note: The tests were calculated using means for specimens from each region separately, and including all species.
Significant or marginally significant results are in bold. For abbreviations, see table 2.
Old and New World Rodent Guilds 489
Table 5: Barton-David test results for the different characters
Trait
G1, 5
G1, 2
P
G1, 4
P
G2, 5
P
.4298
.28781
.3887
.6583
…
…
…
…
.647
.065
.674
.517
.6752
.29282
.4351
.13601
.693
.192
.790
.475
.50925
.35525
.41437
.41756
.067
.194
.132
.129
…
…
…
…
.82776
.84967
.56552
.98031
.094
.081
.278
.010
…
…
…
…
…
…
…
…
…
…
…
…
…
…
…
…
.07255
.23378
.15666
.04397
…
…
…
…
.485
.108
.219
.641
.10641
.28490
.17779
.7341
.560
.201
.376
.671
.48466
.28863
.32358
.39611
.08
.292
.237
.149
…
…
…
…
.85731
.77348
.59771
.92741
.077
.128
.252
.038
…
…
…
…
…
…
…
…
…
…
…
…
…
…
…
…
a
A. Specimens pooled:
Negev:
UTL
IW
CBL
UTRS
Arava:
UTL
IW
CBL
UTRS
B. Specimens measured
in two regions:b
Negev:
UTL
IW
CBL
UTRS
Arava:
UTL
IW
CBL
UTRS
Note: Significant or marginally significant results are in bold. For abbreviations, see table 2.
a
Excluding Psammomys obesus.
b
Measured where Psammomys obesus occurs but excluding this species.
differences between conspecific populations of the different regions.
Sample statistics for the measurements taken for the
different gerbil species are given in table 2. Results of the
B-D tests for pooled data are given in table 3 and for the
unpooled data in table 4. A comparison of tables 3 and 4
shows several significant results, and they tend to be for
the same statistics for the same traits in the same locations.
Thus, for example, for IW, size ratios are significantly similar, as evidenced by G1, n in the Negev and Arava, though
not the Coastal Plain, whether or not the data are pooled.
Second, for all four traits—UTL, IW, CBL, and
UTRS—there are some significant results. For example,
again focusing on G1, n, we see both mean IW and mean
UTL significantly overdispersed (or very close to it) in two
sites, while CBL and UTRS show significance in one site
each.
Results excluding P. obesus are given in table 5 (pooled
and unpooled data, respectively). It is apparent if one compares tables 3 and 5A or tables 4 and 5B that removal of
the fat sand rat changes the results moderately. There are
still significant results but fewer of them. Thus, for example, for pooled data, a highly significant result for the
Arava has much greater null probability with this species
excluded.
The combined probability test of Fisher rarely violated
the independence assumption. For 14 of the 16 tests, no
size ratio (either the smallest or the largest) consisted of
the same species pair for more than one site. For the other
two tests, one ratio (either smallest or largest) consisted
of the same species pair for two of the three sites. These
tests show significance for most traits most of the time
whether or not the data are pooled and whether or not
the fat sand rat is included (table 6).
Results of the two-way ANOVA with trays as repeated
measures show a significant difference in seed preference
between the two species (F p 21.36, df p 4, 110, P !
.0001) in the experiment using commercial seeds of different sizes. The interaction between species and seeds was
significant (F p 20.61, df p 4, 110, P ! .0001). Gerbillus
pyramidum, the larger species, preferred larger seeds,
whereas Gerbillus allenbyi preferred smaller ones (fig. 1).
We performed two-way ANOVAs with nights as repeated measures to test for differences between our replicate experiments and for differences in seed preference
for each seed type separately between the two gerbil species. Our results (table 7) show drastic differences between
rodent species in seed-type choice, a clear difference between replicate experiments for one seed type (Setaria italica), and no significant interactions.
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The American Naturalist
Table 6: Fisher’s combined probability statistic
(associated with x2 test with df p 6) for three
different regions (see text)
Fisher’s statistic
Nominal
probability
UTL
IW
CBL
UTRS
18.316
18.522
12.018
10.435
.005 ! P ! .01
.005 ! P ! .01
.05 ! P ! .1
.1 ! P ! .25a
UTL
IW
CBL
UTRS
21.326
14.010
13.568
11.993
.001 ! P ! .005
.025 ! P ! .05
.025 ! P ! .05
.05 ! P ! .1
UTL
IW
CBL
UTRS
21.193
13.857
10.983
13.893
.001 ! P ! .005
.025 ! P ! .05
.05 ! P ! .1
.025 ! P ! .05a
UTL
IW
CBL
UTRS
15.421
11.145
12.499
10.898
.01
.05
.05
.05
Trait
A:
B:
C:
D:
!
!
!
!
P
P
P
P
!
!
!
!
.025
.1
.1
.1
Note: A, Pooled data, including Psammomys obesus.
B, Separate data, including P. obesus. C, Pooled data,
excluding P. obesus. D, Separate data, excluding P. obesus.
For abbreviations, see table 2.
a
Two of three regions had same pair of species for
one ratio.
from very distantly related families, occur on different
continents.
Upper tooth-row lengths, skull lengths, and tooth-row
surfaces of gerbils in Israel display patterns similar to those
for incisor widths. The overall similarity among the patterns depicted by these characters may result from natural
selection acting on all these traits or from a passive, correlated response to selection directed at incisor size or
other traits (see Dayan et al. 1989b). It may also reflect
foraging behavior. Heteromyid rodents have large, external
cheek pouches in which they collect seeds aboveground
(Reichman 1981); mean pouch volumes of heteromyids
(Morton et al. 1980) also show regular spacing (Dayan
and Simberloff 1994b), much as incisor widths do, while
other traits, including dental ones, show no such patterns.
Gerbillids do not possess cheek pouches, and they seem
to stuff as many seeds as they can into their mouths and
make repeated trips to their burrows or caches (Abramsky
1983). Mandible length, CBL, and tooth-row length may
all provide a rough estimate of the volume available for
seed transport, much as pouch volume does in heteromyids. This possibility may explain the relatively regular
pattern found in these characters and the overdispersed
mean upper tooth-row lengths found by Yom-Tov (1991).
Nonrandom morphological patterns such as these may
arise from species sorting and/or from coevolutionary
change (see Brown and Wilson 1956; Case et al. 1983;
Sinclair et al. 1985a, 1985b; Roughgarden 1989; Dayan and
Our qualitative observations revealed a great difference
between G. pyramidum and G. allenbyi husking behaviors;
large quantities of seed husks were found in the morning
in G. pyramidum seed trays, whereas few seed husks remained in G. allenbyi seed trays.
We performed two-way ANOVAs with nights as repeated measures for the wheat particle–size groups and
found at most a marginally significant difference between
seeds (F p 2.56, df p 2, 51, P p .088), which suggests little or no difference in particle-size choice between the
species. In our samples, the larger species, G. pyramidum,
preferred slightly larger particles than G. allenbyi. No significant difference was found between replicate experiments (F p 1.10, df p 2, 30, P p .345).
Discussion
We found a nonrandom pattern of overdispersed means
for upper incisor widths in three Israeli gerbilline guilds.
This pattern conforms to that found for several heteromyid
rodent guilds of North America. Thus, convergent sizestructured granivorous rodent guilds, composed of species
Figure 1: Seed choice in cafeteria experiment in which Gerbillus pyramidum (white) and Gerbillus allenbyi (black) ate different species of
commercial seeds. Seed size declines from left to right.
Old and New World Rodent Guilds 491
Table 7: Different seed preferences between Gerbillus allenbyi (a) and Gerbillus
pyramidum (p) in cafeteria experiments
Difference
between
replicates
Seed type
Helianthus annuus
Avena sativa
Avena strigosa
Phalaris canariensis
Setaria italica
F
P
Species
favoring
this type
3.22
.05
2.15
.05
14.83
.088
.825
.158
.827
.001
p
p
a
a
a
Species
difference
Interaction
F
P
F
P
28.33
11.13
18.41
10.80
11.18
!.0001
.06
1.20
.85
.08
1.86
.804
.286
.367
.776
.188
.003
.0004
.004
.003
Note: All F ratios have df p 1, 20.
Simberloff 1998). For heteromyids, there is geographic variation in size, and using this variation at the broad regional
scale, we have some indication that the mechanism in play
is coevolution (Dayan and Simberloff 1994b). At the scale
of local coexistence, Bowers and Brown (1982) provide
evidence for species sorting by body size in heteromyids.
There is little geographic variation in size of the gerbillids
in the south of Israel. Therefore, we were unable to use
such variation to understand the relative roles of species
sorting and coevolution in producing the regular pattern
for these gerbillid guilds at the regional scale. Neither are
there data to enable a study of local coexistence analogous
to that of Bowers and Brown (1982).
Whatever the underlying mechanism, the morphological patterns found for North American granivorous rodent guilds and for Israeli gerbillids attest to ecomorphological convergence at the guild level. Both guilds are
size structured for incisor widths, and this morphological
pattern reflects guild organization. Moreover, in recent
years, other studies of both fossil and recent rodent guilds
have demonstrated similar size structuring on the basis of
incisor size (Michaux et al. 1999; Parra et al. 1999).
Incisors of heteromyids are used for husking, some of
which occurs aboveground where predation risk is high
(Rosenzweig and Sterner 1970; Lemen 1978). Therefore,
husking speed may be critical (Rosenzweig and Sterner
1970). Different species exhibit different husking behaviors
related to their body sizes (Lemen 1978), resulting in apparent seed-size selection that is related to body size
(Brown and Lieberman 1973; see also Dayan and Simberloff 1994b). It has also been demonstrated that very
small and very large particles are rejected by heteromyid
rodents (Lawhon and Hafner 1981). Lemen (1978) suggested that interspecific differences in husking behavior
may be explained by an interaction between cheek pouch
size, husking time (which decreases per seed with increasing rodent size; Rosenzweig and Sterner 1970), and exposure to predation.
Abramsky (1983) compared seed-size preference of
some Israeli gerbilline rodents (Gerbillus pyramidum, Gerbillus allenbyi, Gerbillus henleyi, and Meriones crassus) with
that of ants and concluded that both taxa show a preference for large seeds, but he did not study seed-size preferences with a variety of seed sizes among the rodents. Bar
et al. (1984) studied the food habits of gerbilline rodents,
but this study was limited to gross dietary categories. Thus,
seed-size preference of the different species has not been
directly tested in Israel.
Seed-size selection has been studied for North American
heteromyid rodents by cheek pouch contents (Brown and
Lieberman 1973; M’Closkey 1978, 1980) or by seed-choice
preference (cafeteria) experiments in laboratory conditions. In these experiments, researchers used either commercial seeds (Mares and Williams 1977) or hulled, hardwinter red wheat ground to different-sized particles (Price
1983). Because gerbillids do not possess cheek pouches,
we could not examine pouch contents, so we carried out
cafeteria experiments with commercial seeds and with
hulled wheat particles. We hypothesized that, if husking
behavior is key, then seed-size selection would be a factor
in the commercial seed experiment but not in the hulled
wheat experiment.
Results of our experiments with commercial seeds of
different sizes (tables 1, 7) offered in sand trays to G.
pyramidum and G. allenbyi support a hypothesis of seedsize selection in nature: the larger G. pyramidum took
significantly larger seeds than the smaller G. allenbyi. Although the distribution of seed sizes in these sites is unknown, it is likely that most available seeds are smaller
than the commercial seeds we offered. However, the experimental animals readily ate all offered seeds. Research
on heteromyids, summarized by Price and Reichman
(1987), suggests that there are many more small than large
seeds in nature but that several species of rodents select
the large seeds, perhaps to the point of changing the seedsize distribution in the field. Thus, it is quite possible that
partitioning of large seeds by size in an experiment reflects
an important process occurring in nature.
492
The American Naturalist
Figure 2: Choice of wheat particle size by Gerbillus pyramidum (white)
and Gerbillus allenbyi (black) in a cafeteria experiment. Seed size declines
from left to right.
Mares and Williams (1977) believed that using commercial seeds would be preferable to field-collected seeds
because all of the seeds offered were probably unfamiliar
to the rodents; therefore, commercial seeds should minimize the confounding effects of familiarity with wild seeds
that could have caused animals to favor one or another
type of seed because of flavor, consistency, toxicity, or
unknown factors. Further, commercial seeds are generally
selected for little or no toxicity; therefore, this factor would
not interfere with selection for size. The disadvantage of
using commercial seeds is that the seeds differ in taste and
nutritional attributes as well as size (Price 1983). We used
seeds that were totally unfamiliar to the rodents prior to
the experiments and that, as previous experiments indicated (Rahmut Ben-Moshe 1996), were palatable to both
species. Since these closely related gerbil species are very
similar in their biology, their seed choices are expected to
be similar, and seed size should be the major factor. No
significant difference in seed-size choice was found in the
hulled-wheat experiment, in which the food particles required no treatment.
Abramsky et al. (1991) concluded by direct observations
that G. allenbyi exhibits different foraging behaviors under
laboratory and field conditions. In the laboratory, this gerbil ate the seeds on the seed trays and did not collect and
cache them, whereas in the field, it collected seeds in its
mouth without eating them to transport them frequently
to burrows. In our experimental setup, under simulated
natural conditions in which perceived risk of predation is
considerable, gerbils did husk some of the seeds in the
seed trays. This was particularly true for the larger G.
pyramidum, which were also taking larger seeds. Thus, the
rationale for selection on incisor width of gerbils parallels
our rationale for heteromyid rodents (Dayan and Simberloff 1994b).
Dayan and Simberloff (1994b) suggested that, if husking
large seeds by small species necessitates staying exposed
for a relatively long time at a particular place, the energetic
advantage of taking this large seed may be outweighed by
excessive risk of predation. In other words, there may be
a trade-off between husking large seeds (which takes time
aboveground), so as to carry more of them per foraging
trip, and not husking them, thereby requiring more trips.
Aboveground husking speed may be critical to these rodents. This hypothesis implies there may be considerable
overlap in the intake of smaller seeds between the different
species. In fact, Brown and Lieberman (1973) and Mares
and Williams (1977) emphasized for heteromyids that it
is the increased tendency of large species to select large
seeds (in addition to many small seeds) that gives rise to
their high average seed sizes. They suggested that this tendency gives the larger species a competitive advantage. In
our experiment, combining data from table 1 and figure
1, we found the larger G. pyramidum to take larger seeds
on average than G. allenbyi (length: 11.87 vs. 8.10 mm);
similarly, using data from figure 2, we found G. pyramidum
to take slightly larger ground seed particles than G. allenbyi
(2,470 vs. 2,408 m). Larger species are frequently found to
have a larger food-range size among particulate feeders
(Schoener 1969; Wilson 1975). In our experiment with
commercial seeds of five species, G. pyramidum took similar amounts of large and small seeds, while the smaller
G. allenbyi took a much smaller amount of large than of
small seeds (fig. 1). In the ground wheat experiment, with
much smaller particles overall, the two species took similar
proportions of the different-sized particles, although the
larger G. pyramidum took slightly larger particles on average (fig. 2).
In heteromyid rodents, the hypothesis of seed-size selection, at first supported by cheek pouch content sieving
and feeding experiments (Brown and Lieberman 1973;
Mares and Williams 1977), was later challenged by other
studies (e.g., Smigel and Rosenzweig 1974; Lemen 1978;
M’Closkey 1978, 1980; Price 1983; but see Dayan and
Simberloff 1994b). Increasingly, other mechanisms facilitating coexistence, such as differing microhabitat preferences, seed dispersion preferences, trade-offs in the foraging efficiencies of different granivorous species, and
interference competition (reviewed by Brown [1987], Kot-
Old and New World Rodent Guilds 493
ler and Brown [1988], and Brown et al. [1994]), have been
emphasized. Microhabitat selection has also been considered to be key to coexistence among Israeli gerbils (Rosenzweig et al. 1984; Abramsky et al. 1985, 1990, 1991).
Another mechanism recently emphasized for gerbils is
temporal partitioning (Kotler et al. 1993; Ziv et al. 1993),
emphasizing that coexistence may be facilitated by more
than one axis of heterogeneity.
While the occurrence of interspecific competition has
been demonstrated unequivocally in both heteromyids and
gerbillids, it does not necessarily follow that competition
will affect community structure (cf. Stone et al. 1996) or
that it will do so in the same way in both rodent communities. Historical factors may strongly influence community structure, so that, although common processes of
community assembly may operate, they may do so to very
different degrees (Kelt et al. 1996). Our results suggest that
seed-size selection is a further mechanism facilitating coexistence among Israeli gerbillines and North American
heteromyids. We found size-structured seed-eating rodent
guilds among gerbillines, as among heteromyids, attesting
to convergence in mechanisms structuring community
morphology between Old and New World granivorous
desert rodents.
Acknowledgments
We thank Z. Abramsky, B. Kotler, J. Losos, and Y. YomTov for constructive suggestions on earlier drafts of this
manuscript. A. Landsman provided technical assistance,
while B. Kotler allowed us to use his aviary and L. OlsvigWhittaker let us use her sieving machine.
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Associate Editor: Jonathan B. Losos