How not to write in
defense of threatened tortoises
Yehudah
L. Werner
Department of Evolution, Systematics
and Ecology, The Hebrew University of Jerusalem, 91904
Jerusalem, Israel
Email: yehudah_w@yahoo.com
Date of publication (online): 26
September 2009
Date of publication (print): 26
September 2009
ISSN 0974-7907 (online) |
0974-7893 (print)
Editor: Aaron Bauer
Manuscript details:
Ms # o2251
Received 06 July 2009
Final received 22 August 2008
Finally accepted 31 August 2009
Citation: Werner, Y.L.
(2009). How not to write in defense of threatened tortoises.
Journal of Threatened Taxa 1(9): 471-473.
Copyright: © Yehudah L. Werner 2009. Creative Commons Attribution 3.0 Unported License. JoTT allows
unrestricted use of this article in any medium for non-profit purposes,
reproduction and distribution by providing adequate credit to the authors and
the source of publication.
Author Details: Yehudah L. Werner has participated
in founding the Society for the Protection of Nature in Israel; taught, in
various capacities, vertebrate zoology and herpetology at the Hebrew University
of Jerusalem during 1953-1999; and edited the Israel Journal of Zoology during
1973-1989. As Professor Emeritus he
continues to research.
Acknowledgements: I thank Dorothee Huchon, Gila Kachila, Tal Pupko and Herve Seligmann for enlightening
inputs, although not all of it could be accommodated here.
Abstract: Prudent
use of the limited conservation resources rests on solid taxonomy data. This is a critical review of a taxonomy paper
aimed at conservation but in itself not fully reliable (“Genetic evidence for
premature taxonomic inflation in Middle Eastern tortoises”, Parham et al.,
2006, Proc. Calif. Acad. Sci. 57: 955–964). Its authors consider that
unjustified naming of species is detrimental to conservation. This reviewer considers the paper flawed in
(a) selection and reportage of voucher specimens, partly erroneous or
inaccurate; (b) methods; (c) scientific reasoning and conclusions; and (d)
clarity of argumentation. Hence even if the results are supported by the more
solid results of others, the paper in itself is considered not to be
sufficiently reliable for systematics or
conservation.
Keywords: Conservation,
DNA, Middle East, morphology, systematics, taxonomy, Testudo floweri, Testudo graeca, Testudo werneri
Abbreviations: MVZ
- Museum of Vertebrate Zoology, University of California at Berkeley.
Introduction
Scientists comprise architects and
bricklayers but the bricklayers depend upon the solidity of available
bricks. Conservation relies on
biodiversity data, primarily identification of taxa
and definition of distribution ranges (Meffe &
Carroll 1997; Samper 2004; Secretariat of the Convention on Biological
Diversity 2008). Here I analyze a
taxonomic brick that seems insufficiently solid for the conservation effort for
which it was manufactured, tortoise conservation in the Mediterranean basin, a
global biodiversity hotspot for reptiles (Baha El Din
et al. 2008). Even if some conclusions
are externally supported, and indeed some are by Fritz et al. (2007), the paper
in itself seems problematic. From its
scientific reasoning down to punctuation this paper seems spattered with
inaccuracy, while in science, as in court, inaccuracy of a witness degrades the
evidence. I can give here only some
examples.
The Spur-thighed
Tortoise, Testudo graeca
Linnaeus, 1758, is widespread across the ecologically heterogeneous
Mediterranean basin and shows geographical variation. Local populations have
been morphologically recognized as species or subspecies, amounting to 17
nominal subspecies (Fritz & Havaš 2007). The validity of some has been contested on
molecular grounds (Fritz et al. 2007), rendering conservation priorities a
matter of scientific philosophy.
Conservation is necessary because many of these populations have been
over-exploited, by amateurs (Pérez et al. 2004), the
pet trade (Lambert 1979, 1981, 1984), and for food (Beshkov
1993).
Observations and Comments
The paper reviewed (Parham et al. 2006a)
aimed “to provide a genetic test for the newly recognized morphology based
taxonomy in Middle Eastern T. graeca using a
rapidly evolving molecular marker and specimens with well-documented locality
data.” Using phylogenies the authors concluded a recommendation to avoid using
some “new” taxon names, including Testudo
floweri Bodenheimer,
1935, despite admitting that taxa dropped might be
revalidated by additional research.
The methodology of calculating
phylogenies suffers the weakness that results depend on outgroups
commonly chosen by less objective considerations. Parham et al. (2006a) overcame this by
deriving outgroups from earlier results (Parham et
al. 2006b). But the outgroups
for that project had been chosen by those non-objective considerations. Moreover, one outgroup, Testudo
kleinmanni, was based on a seemingly dubious
voucher (see below).
The introduction is confusing, defining
“taxonomic inflation” as the promotion of many subspecies to species but
accusing it of introducing unfamiliar names.
How so, if most were familiar subspecies names?
The authors seem to care for
conservation but the paper’s contribution remains unclear unless one reads the
cited literature. In the Introduction’s
second paragraph the group is assigned conservation concern but this is not
linked with the paper’s aim. The
Abstract does say that “an accurate understanding of major evolutionary
lineages in this taxon is important for guiding
conservation strategies” but this is not supported in the text. The Conclusions suggest that reducing
taxonomic changes and unjustified taxa benefits
conservation through improving the credibility of taxonomy. But the paper contains no foundation for this
conclusion and it remains enigmatic what the benefits for conservation should
be if a monotypic Testudo graeca were recognized, ranging from North Africa to
Central Asia.
I agree with Parham et al.’s (2006a)
attitude, that congruence of molecular and morphological distinction would
support the taxa distinguished. But I do not agree that incongruent molecular
and morphological variation, or overall low sequence divergence, must
necessarily discredit any morphologically-distinguishable taxa
compared, as done by them. Parham et al. (2006a) used “rapidly-evolving”
portions of the mitochondrial DNA. This
evolution is independent of selective pressures. Rates of DNA and phenotype
evolution are separate (Bromham et al. 2002; Davies
& Savolainen 2006). One cannot disregard a
potential scenario that two populations, recently physically separated, diverge
under different selective pressures, leading to visible speciation that has
outraced the monotonously evolving mtDNA. Such speciation could be expressed in
untested parts of the genome. Another scenario for mtDNA
comparisons failing to distinguish species derives from hybridization (Smith et
al. 2008).
These potential scenarios reflect a
truism. The lack of evidence from one
character-group (here, partial DNA evidence) cannot automatically overrule
evidence from another character-group (here, morphology). It is not easy to derive “does not exist”
from “not observed”. Specifically, DNA
notwithstanding (Parham et al. 2006a; Fritz et al. 2007), I find it hard to
lump the tortoises of the Golan plateau and of the adjacent Galilee, Israel,
the former being larger, darker and more corrugated than the latter (Sivan
& Werner 1992). Could these
differences reflect environmental effects on embryogenesis (Fox 1948; Werner
1961; Deeming 2004; Qualls & Shine 1998) ? The data available for chelonians (Du & Ji 2003; Deeming 2004) fail to explain these morphological
differences.
Under Materials, one outgroup,
Testudo kleinmanni,
is based on a single specimen of unknown origin. Its number, “MVZ 230361” (also in Parham et
al. 2006b), actually belongs to a salamander in the MVZ’s catalogue. Although listed in the material, this species
is missing from the appendix of Parham et al. (2006a) that provides specimen
details.
The selection of ingroup
material seems unfortunate, particularly regarding the question whether the
name T.g. floweri
is justified. Incidentally, as
subspecies (Hoofien 1967; Werner 1988) it is not
involved in taxonomic inflation. The map
(fig. 1) lacks geographical degrees and scale bar but the distance between the
sampled type localities of T. floweri
in the south and T. antakyensis and T. terrestris in the north approximates 600 km. Although
in this area such a South-North gap implies a dramatic ecological jump (Yom-Tov & Tchernov 1988), this
interval was not sampled. Had T. floweri differed from these northern samples, it
would have been tantalizing not to know the affiliation of the intervening
populations.
The quantitative sampling of localities,
usually N=1 per site, is surprising. If
a character varies between two related taxa, it is
likely to have varied within the common ancestral population. Indeed, characters that are stable and
distinguish between some species, may vary within
another species. Working with morphological characters, nobody would compare
species without heeding intraspecific variation. In this respect it would have been sounder to
adopt the strategies of Attum et al. (2007), Fritz et
al. (2007) and Široký & Fritz (2007) in
DNA-verification of Testudo taxonomy.
The restriction of the sample of the
questioned T. floweri to N=1 is particularly
problematic. Its collection locality in
the MVZ web-posted catalogue, “near Newe Deqalim, Southern Gaza Strip” is inaccurate. The locality was “Probably near Newe Deqalim, etc.”. The specimen, and another likewise deposited in MVZ but not
utilized, were among tens collected by children and maintained by Mr. Eli
Moses, Newe Deqalim, the
“proxy collector”. Mr. Moses, with the
mediation of Dr. Ran Lapid, gave the specimens to me
for sending to Parham and coauthor Papenfuss. I transmitted Mr. Moses’s
explanation that generally the tortoises originated from the vicinity but some
may have been brought from elsewhere. Papenfuss considered this good enough. It would have been, had the results shown a
difference. But for a negative result, the second, wasted, individual should
have been sequenced. The probability
that both were extralimital could be considered
negligible.
Entering Parham, who only received the
turtles from me, into the MVZ catalogue as collector, ignores the collector’s
roles as witness for the collection data and as source for details.
Moreover, the work with T. floweri has a worse flaw. Parham et al. (2006a) considered the type
locality to be the Gaza Strip. But Bodenheimer (1935)
had described the taxon from the “Negev” and his book
contains a map that specifically excludes the Gaza strip from the Negev.
The Methods (Parham et al. 2006 a,b) ignore a point that most
journals now require: how were the animals treated, and how were they
killed? Space precludes reporting on
faults at the copy-editing level.
Conclusion
In summary the paper is at all levels
not sufficiently accurate to be considered a reliable brick that could in
itself contribute to turtle taxonomy and conservation.
References
Attum, O., S. Baha El Din, S. Carranza, R. Earley,
E.N. Arnold & B. Kingsbury (2007). An evaluation of the
taxonomic validity of Testudo werneri. Amphibia-Reptilia
28: 393-401.
Beshkov, Vl. (1993). On the distribution,
relative abundance and protection of tortoises in Bulgaria. Chelonian
Conservation and Biology 1(1): 53-62.
Bodenheimer, F.S. (1935). Animal Life
in Palestine.,
L. Mayer, Jerusalem.
Bromham,
L., M. Woolfit, M.S.Y. Lee & A. Rambaut (2002). Testing the
relationship between morphological and molecular rates of change along
phylogenies. Evolution 56: 1921-1930.
Davies, T.J. & Y. Savolainen (2006). Neutral
theory, phylogenies, and the relationship between phenotypic change and
evolutionary rates. Evolution 60: 476–483.
Deeming,
D.C. (2004).
Post-hatching phenotypic effects of incubation in reptiles,
pp. 229-251. In: Deeming, D.C. (ed.). Reptilian
Incubation: Environment, Evolution and Behaviour.
Nottingham University Press, Nottingham.
Du, W.-G. & X. Ji (2003). The effects of incubation thermal environments on size, locomotor performance and early growth of hatchling soft-shelled
turtles, Pelodiscus sinensis.
Journal of Thermal Biology 28: 279–286.
Fox,
W. (1948).
Effect of temperature on development if scutellation
in the garter snake, Thamnophis elegans atratus. Copeia 1948: 252-262.
Fritz,
U. & P. Havaš (2007). Checklist of chelonians of the world. Vertebrate Zoology
57: 149-368.
Fritz,
U., A.K. Hundsdörfer, P. Široký,
M. Auer, H. Kami, J. Lehmann, L.F. Mazanaeva, O. Türkozan & M.
Wink (2007).
Phenotypic plasticity leads to incongruence between morphology-based taxonomy
and genetic differentiation in western Palaearctic
tortoises (Testudo graeca
complex; Testudines, Testudinidae).
Amphibia-Reptilia 28: 97-121.
Hoofien, J.H. (1967). An alphabetical list of the reptiles of Israel according to the
status on May 31st, 1967. Department
of Zoology, Tel-Aviv University, Tel Aviv.
Lambert, M.R.K. (1979). Trade and the Mediterranean tortoises. Oryx 15:
81–82.
Lambert, M.R.K. (1981). Temperature, activity and field sighting in the Mediterranean spur-thighed or common garden tortoise Testudo
graeca. Biological Conservation 21:
39-54.
Lambert, M.R.K. (1984). Threats to
Mediterranean (West Palaearctic) tortoises and their
effects on wild populations: an overview. Amphibia-Reptilia
5: 5-15.
Meffe,
G.K. & C.R. Carroll (eds.) (1997). Principles
of conservation biology. Sinauer,
Sunderland, Massachusetts.
Parham,
J.F., O. Türkozan, B.L. Stuart, M. Arakelyan, S. Shafei, J.R. Macey, Y.L. Werner & T.J. Papenfuss
(2006a).
Genetic evidence for premature taxonomic inflation in Middle
Eastern tortoises. Proceedings of the California Academy of Science 57:
955–964.
Parham,
J.F., J.R. Macey, T.J. Papenfuss,
C.R. Feldman, O. Türkozan, R. Polymeni
& J.L. Boore (2006b). The phylogeny
of Mediterranean tortoises and their close relatives based on complete
mitochondrial genome sequences from museum specimens. Molecular Phylogenetics and Evolution 38: 50–64.
Pérez, I, A. Giménez, J.A. Sánchez-Zapata,
J.D. Anadón, M. Martínez
& M.A. Esteve (2004). Non-commercial
collection of spur-thighed tortoises (Testudo graeca graeca): a cultural problem in southeast Spain. Biological
Conservation 118: 175–181
Qualls,
F.J. & R. Shine (1998). Geographic variation in lizard phenotypes:
importance of the incubation environment. Biological Journal of the Linnaean
Society 64: 477-491.
Samper, C. (2004). Taxonomy and environmental policy. Philosophical Transactions of the Royal
Society of London B 359: 721–728.
Secretariat of the Convention on
Biological Diversity (2008). Guide to the global taxonomy
initiative. Technical Series no. 30, Montreal, Canada.
Široký,
P. & U. Fritz (2007). Is Testudo
werneri a distinct species? Biologia,
Bratislava 62: 228-231.
Sivan, N. & Y.L. Werner
(1992). Survey of the reptiles of the Golan Plateau and
Mt. Hermon, Israel. Israel Journal of
Zoology 37: 193-211. Publishing
Smith, M.A., N.A. Poyarkov,
Jr. & P.N.D. Hebert (2008). CO1 DNA barcoding
amphibians: take the chance, meet the challenge. Molecular Ecology Resources
8: 235–246.
Werner,
Y.L. (1988).
Herpetofaunal survey of Israel (1950-85), with comments on Sinai and Jordan and
on zoogeographical heterogeneity, pp. 355-388. In: Yom-Tov, Y. & E. Tchernov (eds.). Zoogeography of Israel.
Monographiae Biologicae 62,
W. Junk, Dordrecht.
Yom-Tov, Y. & E. Tchernov (eds.)
(1988).
Zoogeography of Israel, Monographiae
Biologicae 62 W. Junk, Dordrecht.