Hobbits from the Deep South: Historical Drivers of

Dwarfism in Modern Antarctic bivalves

1

Marcelo M. Rivadeneira , Jaime A. Villafaa , Sandra Gordillo , Sol Bayer & Sven N. Nielsen
1 Laboratorio de Paleobiologa, Centro de Estudios Avanzados en Zonas ridas (CEAZA), Coquimbo, Chile
2 Centro de Investigaciones en Ciencias de la Tierra, Consejo Nacional de Investigaciones Cientficas y Tcnicas
(CICTERRA, CONICET-UNC) & Centro de Investigaciones Paleobiolgicas (CIPAL), Facultad de Ciencias Exactas, Fsicas y
Naturales, Universidad Nacional de Crdoba, Crdoba, Argentina
3 Instituto de Ciencias de la Tierra, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile
* email:

marcelo.rivadeneira@ceaza.cl

Abstract. The modern Antarctic bivalve fauna has long

been considered as unusually small-sized or dwarf.
However the validity of this pattern and the underlying
causes remain little studied. We used a worldwide
compilation of body sizes of 5185 bivalve species across
17 major biogeographic provinces to show that Antarctic
species are statistically smaller than in any other province,
a pattern not attributable to sampling artifacts. The
available fossil record shows that dwarfism may have
existed since the Oligocene-Neogene, after the onset of
glaciation, highlighting the importance of historical
processes. Indeed, models show that dwarfism cannot be
linked to present-day ecophysiological or ecological
restrictions, but rather to the unusual bathymetric patterns
of species. Our numerical experiments support the idea
that the combined effect of the extinction of large-sized
shallow-water forms, and the subsequent invasion of smallsized deep-water species has shaped the dwarfism of
Antarctic bivalves at evolutionary timescales. This
mechanism may further provide an explanation for the
extreme body sizes in Antarctic organisms in general.
Palabras

Claves: Body size, ecogeographic

macroecology, biogeography, Cenozoic

traditionally been attributed to ecophysiological

adaptations to contemporaneous conditions (Arnaud 1977,
Moran and Woods 2012). However, two evolutionary
hypotheses have been proposed to highlight the relevance
of historical processes shaping the Antarctic dwarfism. The
biogeographic dynamics hypothesis relies on the wellestablished similarity between Antarctic and deep-sea taxa.
The body size of abyss bivalves is typically much smaller
than shallow water forms which combined with the marked
eurybathy of Antarctic taxa (Dell 1972) may lead to the
prevalence of small-sized assemblages. Finally, the clade
dynamic hypothesis implies than dwarfism is a clade-level
phenomenon induced by size-dependent diversification
patterns than favored and enhanced speciation and/or
reduced extinction of small-sized forms. Here we put these
ideas to a test, first validating the existence of dwarfism as
a phenomenon observed in Antarctic bivalves and then
evaluating to which extent dwarfism can be explained by
evolutionary processes.

rules,

2 Methods

1 Introduction

2.1 Methods

Polar regions offer an excellent arena for the study of

patterns and processes shaping body sizes of biotas, given
the remarkable existence of gigantism and dwarfism in
several taxa (Nicol 1970, Arnaud 1977). Polar gigantism
has been reported in foraminifera, sponges, ctenophores,
polychaetes, cephalopods, copepods, isopods, amphipods,
pycnogonids, and echinoderms (Moran and Woods 2012).
The contrary phenomenon, dwarfism, has been described
mainly for Antarctic taxa including brachiopods, chitons,
prosobranch gastropods, bivalves, and fishes (Moran and
Woods 2012). The unusual Antarctic dwarfism in bivalves
has been noticed since more than four decades (Nicol
1970, Arnaud 1977, Valentine et al. 2006): more than 60 %
of species reach a maximum shell length 10 mm, two or
three-fold less than observed in the Arctic region (Nicol
1970, Arnaud 1977). Contrary to the fascination drawn by
gigantism and the study of its causes, however, the
underlying mechanisms of dwarfism are much less
understood.

Body size information, first description year, geographic

distribution, and bathymetric distribution were obtained
for 5185 present-day species belonging to 91 families from
Hubers Compendium of Bivalves (Huber 2010). Body
size was estimated as maximum size known (i.e. largest
extension of the shell). Body size was also obtained for
Cenozoic fossil assemblages based on a comprehensive
literature compilation, following the most recent
taxonomic criterion (Beu 2009). Most of the fossil data
comes from the Paleocene and Eocene outcrops of
Seymour Island and McMurdo Sound (Stilwell and
Zinsmeister 1992, Stilwell 2000, Stilwell et al. 2004) (97
putative species). The Oligocene and Neogene record
(Gazdzicki and Pugaczewska 1984, Anelli et al. 2006) is
much less diverse (33 putative species) and preserved and
so the inventory should be considered as preliminary. We
have to stress that face-value comparisons of fossil versus
present-day body sizes may likely yield incorrect results
because of the inherent bias in the fossil record (i.e. small
sizes are less likely represented) (Cooper et al. 2006,
Valentine et al. 2006). However, in our case this bias goes

The existence of body size extremes in the Antarctica have

against our predictions, and hence the test is actually much

more conservative. Indeed, the similarities in the
frequency distributions of body sizes between Recent and
the comparatively incomplete Oligocene-Neogene record
suggests that fossil bias should not mask overall temporal
trends.
To evaluate the importance and interaction between
biogeographic and phylogenetic (clade) factors affecting
Antarctic body size we carried out different numerical
experiments. We compared the observed cumulative
frequency distribution of modern and fossil (Paleogene,
Oligocene-Neogene) Antarctic bivalves with the
expectations of five different null models; a) shallow
water: random resampling from shallow water areas
(shelves, 200 m depth) of the global ocean (excluding
Antarctica), b) deep water: random resampling from deep
water areas (slope and abyss, > 200 m depth) of the global
ocean, c) clade: random resampling from the same families
represented in Antarctica, d) shallow water + clade:
stratified resampling from the same families represented in
Antarctica shallow but restricted to shallow water areas of
the global ocean, and e) deep water + clade: stratified
resampling from the same families represented in
Antarctica shallow but restricted to deep water areas of the
global ocean. 10,000 runs were used for each model.
Observed versus predicted curves were compared using
Kolmogorov-Smirnov tests. The proportion of nonsignificant tests was used as a pseudo-r2, i.e. measure of
the ability of the null model to reproduce observed curves.
All analyses were run using scripts written in R (Team
2014).

Body size shows a distinctive reduction during the

Cenozoic, declining from the Paleogene to the recent (Fig.
1A). The size of Paleogene bivalves was statistically
different to Neogene and Recent assemblages (KS-test, D=
0.362, P = 0.003 and D = 0.487, P < 0.0001, respectively),
with a median value of 38 mm, 4.5-fold higher than the
recent counterpart. However, size of Recent bivalves was
not different to the Neogene (KS-test, D = 0.23, P =
0.131). The numerical experiments showed that null
models accurately reproduce the frequency distribution of
body sizes of both Recent and Paleogene Antarctic
bivalves (Fig. 1B, C). Recent Antarctic bivalves are similar
to the fauna inhabiting deeper areas of the global ocean
(modern-deep model; pseudo-r2 = 0.89). Controlling for
phylogenetic effects increases the accuracy of the model
(modern clade + deep model; pseudo-r2 = 0.98, AICw =
0.54, Fig. 1B). In both cases, the observed median and
75th percentile of body size were not different than
predicted by these models. Models assuming a re-sampling
from shallow-water areas, or pure clade effects performed
poorly. The numerical experiments showed that body size
of Paleogene bivalves can be well predicted by fossil clade
and fossil deep models; size is very similar to species
inhabiting the shallow water habitats (fossil shallow
model; pseudo-r2 = 0.76, AICw = 0.29), and to modern
species belonging to those families present during the
Paleogene (fossil clade model; pseudo-r2 = 0.55, AICw =
0.21). The precision decreased combining bathymetric and
clade effects (fossil clade + shallow model; pseudo-r2 =
0.64, AICw = 0.23, Fig. 3C).

3 Discussion
2.2 Results
Antarctic bivalves are the smallest among all 17
biogeographic provinces analyzed when comparing the
median, 95th percentile and maximum body size (Table 1).
The median body size of Antarctic bivalves reaches only 8
mm, and 95% of species are smaller than 83 mm. The
frequency distribution of Antarctic bivalves is different to
any other province (Kolmogorov-Smirnov test, p < 0.0001
in all cases, Table 1). In contrast, the median size of Arctic
bivalves is 5-fold larger (32 mm), and its overall frequency
distribution is not different to that observed in the warm
and highly diverse Caribbean province (KS-test, D= 0.07,
P = 0.78). The smaller size of Antarctic bivalves cannot be
attributed to size-bias in the completeness of species
inventories. Differences between Antarctic and other
provinces remained firm even after including only those
species described before 1950 or 1900 (Table 1). The sole
exceptions are the comparison with the Mediterranean and
Boreal provinces, which before 1900 showed a size
structure similar to the Antarctic province (Table 1). By
1950 the frequency distribution of Antarctic bivalves was
already similar to that of today (KS-test, D= 0.06, P =
0.99) with a median of 9 mm, quite close to the actual 8
mm.

Antarctic bivalves break down two well-known

biogeographic patterns: the Bergmanns and Copes rules.
One the one hand, our results confirm that Antarctic
bivalves are much smaller than those in any other region
across global oceans, validating a pattern suggested more
than four decades ago (Nicol 1970).
Our results also suggest that dwarfism has existed at least
since the Miocene, implying a sort of reverse Copes rule
in Antarctic bivalves during the Cenozoic, contrary to the
trend observed in other marine organisms (Schmidt et al.
2004, Hunt and Roy 2006). The precise timing of the
miniaturization of bivalve biota cannot be stated without
further paleontological work. It appears, however, to be
coeval with the onset of the Antarctic glaciation, during the
Eocene-Oligocene at ca. 32 Ma (Zachos et al. 2001). The
body size reduction is also reminiscent of the so-called
Lilliput effect (Twitchett 2007, Keller and Abramovich
2009), i.e. a drastic reduction in the body size of
invertebrates after a major extinction, because the advance
of glacial armadas over the coastal shelf must have
produced a large demise in diversity of shallow-water
forms (Thatje et al. 2005).

The Antarctic dwarfism is consistent with the historical

(i.e. biogeographic and evolutionary) rather than
contemporaneous (i.e. ecophysiological) hypotheses. The
mean shallowest bathymetric limit of Antarctic bivalves
(100 m) is unusually deep, more than three-fold deeper
than in any other biogeographic province in the world (30
m on average). Hence, the prevalence of small-sized forms
could be directly linked to a two-step process: i) the
extinction of Paleogene coastal shelf fauna, and ii) the
advance of deep-water forms towards the shelf. This idea
is reinforced by the fact that bivalve body size prior to the
onset of Antarctic glaciation was similar to shallow-water
assemblages across the world. The advance of minute
deep-water forms towards the species-impoverished
coastal shelf should took place particularly during interglacial times when ice lobes retreated from the shelf
(Thatje et al. 2005). This was likely favored by the unique
great depth of the Antarctic shelf, reaching ca. 500 m in
average, molded by glacial loading and erosion
(Andriashev 1965, Vanney and Johnson 1985). Our
numerical experiments also suggest that the importance of
clade effects varied in time. Models including clade effects
successfully reproduced the body size of Paleogene
bivalves, supporting a family-level selectivity of postPaleogene faunal turnover that took away larger forms
(Krug et al. 2010). In contrast, clade effects alone cannot
explain modern dwarfism, suggesting that the recolonization or shelf re-invasion from deep waters was
largely a taxonomically non-selective process.
The biogeography model provides a unified framework to
understand body size extremes in Antarctic organisms;
groups showing increasing body sizes towards abyssal
zones (e.g. isopods, pycnogonids and amphipods)
(Timofeev 2001, Moran and Woods 2012) are Antarctic
giants, whereas taxa decreasing body sizes towards abyssal
zones (e.g. gastropods) are typically dwarfs (McClain et al.
2006). Future phylogenetic information combined with
more exhaustive paleontological surveys in Neogene
deposits may shed light on the processes leading to the
establishment of modern dwarfs and giants in Antarctica.

Aknowledgement
This work was funded by INACH grant G_05-11.

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Table 1 . Body size structure of bivalve species in 17 marine biogeographic provinces. Also shown differences (Kolmogorov-Smirnovs
D) in the frequency distribution of bivalve body size between Antarctic and the other 16 biogeographic provinces, accordingly to the year
of taxonomic description of the species (before 1900 or 1950). Significant values (p < 0.05) are indicated in bold. ns: non significant (p >
0.05).
Size (mm)
Species
analyzed

Minimum

Antarctica

115

Magellan

118

23

Province

th

median

Antarctic versus other provinces (D)

95

th

Maximum

All Species

Before 1950

Before 1900

83

145

116

244

0.309

0.350

0.338

Argentinean

192

20

102

244

0.250

0.387

0.298

New Zealand

366

15

137

405

0.237

0.267

0.438

South Africa

278

22

100

390

0.296

0.353

0.332

South Australia

350

18

115

372

0.246

0.251

0.352

Peruvian

132

38

155

600

0.457

0.495

0.469

West Africa

398

26

121

565

0.355

0.438

0.335

Indian

1905

33

132

1369

0.425

0.452

0.451

Caribbean

585

21

123

395

0.282

0.311

0.223

Panamic

558

41

142

600

0.498

0.497

0.520

Hawaiian

117

28

151

300

0.385

0.368

0.411

Japanese

766

35

150

621

0.461

0.511

0.468

Mediterranean

443

21

119

1200

0.294

0.331

0.233

ns

Boreal

85

18

167

370

0.229

0.225

0.155

ns

Aleutian

109

32

176

288

0.405

0.436

0.413

Arctic

115

26

141

200

0.339

0.356

0.287

Figure 1. A) Changes over time in the cumulative frequency distribution of body sizes of Antarctic bivalves from the Paleogene to the
Recent. Predicted body size of bivalves in recent (B) and Paleogene assemblages (C), accordingly to the best null models (clade + deep
water, and clade + shallow water, respectively,).