Literature survey , bibliographic analysis and a taxonomic catalogue of subterranean fauna from Portugal

A bibliographic analysis of the hypogean biological studies in Portugal is made, compiling 138 publications related to the subterranean invertebrate fauna, since its begining in 1870 until November 2012. A catalogue of hypogean endemic taxa is provided, listing 27 troglobionts and 63 stygobionts, described to be obligate hypogean and endemic from mainland Portugal (Macaronesian archipelagos excluded). The first impetus on troglobiont studies was provided by the prospections of Barros Machado during 1940’s and by an expedition of Lindberg in the spring of 1961; and the major information about stygobiont species was provided by the former Instituto de Zoologia “Dr. Augusto Nobre” from Porto University.


INTRODUCTION
A literature survey allows a critical assessment of the state of subterranean biology, and is a crucial labor to put order in the knowledge of the hypogean fauna, and to avoid repetition of research due to the difficulties of getting information in old bibliographical sources (Fan 2006).
The subterranean habitat harbours an extremely specialized fauna, being a true laboratory for the study of ecology, natural selection and evolution, central subjects in biology (Culver & Pipan 2009).The study of the subterranean fauna began limited to the perspective of 'human size' caves as the domain of the cave-dwelling fauna (Vandel 1964), but the evolution of knowledge in subterranean biology leads to a broad view of the subterranean habitats as a large variety of places with aphotic conditions, extending their limits far beyond the caves (Pipan & Culver 2012).
The first published register of subterranean fauna from Portugal (Chiroptera excluded) was in the monography "Trechorum oculatorum" where specimens of a ground beetle collected by Schaufuss in portuguese caves were recorded by Putzeys (1870: 18).The specimens were assigned to Trechus fulvus Dejean, 1831 in spite of exhibiting a larger and more rounded pronotum than is proper to this species, and neither the caves nor the geographic area of Portugal were specified.
The first hypogean taxon described from Portugal was the troglobiont spider Nesticus lusitanicus Fage, 1931, based on specimens collected during a cave survey and exploration by the archaeologist Henri Breuil and the geologist Ernest Fleury, in the beginings of the last century (Gama & Afonso 1994).
The great momentum in the history of Portuguese subterranean biology was given by António de Barros Machado, an eminent arachnologist that began methodical exploration of caves in Portugal in the late 1930's.He performed an intense sampling effort on terrestrial hypogean fauna along the karstic caves of Portugal, and co-authored by his brother Bernardino de Barros Machado described more than 300 caves in the "Inventário das cavernas calcárias de Portugal".In the same decade, Fernando Frade from Lisbon University described Proasellus lusitanicus (Frade, 1938) from the Alviela spring in the Estremenho karst massif, paving the way for the study of stygobionts in the following decades by researchers of the former Instituto de Zoologia "Dr.Augusto Nobre" from Porto University.
Most of the biological hypogean studies in Portugal have been done in caves and dark wells.A large cryptic biodiversity still remains to unravel, especially in the mesocavernous shallow substratum (MSS as described by Juberthie et al 1980) and in the anchialine waters of coastal karsts.
More recently several efforts by Reboleira and colleagues, among others, to access subterranean biodiversity in Portugal in karst areas are providing new interesting information (Reboleira et al 2011).

METHODS
The entire bibliography on Portuguese subterranean biology has been revised (excluding that on Macarone-sian archipelagos and references to Chiroptera) since the first publication in 1870 until November 2012.
The term hypogean is used for the species that live exclusively in subterranean habitats beneath the soil layers, displaying clear adaptations to the subterranean environment, expressed morphologically as convergent evolution, such as integument depigmentation, absence or reduced ocular structures, elongated appendages, and wing reduction in insects.The endogean fauna occurring inside the soil is excluded of the aim of this catalogue.

RESULTS
As much as 138 scientific publications have been published between 1870 and November 2012, dealing on the hypogean fauna of mainland Portugal, from where 27 troglobiont and 63 stygobiont species have been described so far (see Table 1 and 2 for taxonomic information).
Chronologically, the proportion of higher number of publications is not necessarily the result of higher number of new described taxa (Fig. 1).
The decade of 1960 was the most productive in number of such publications, but the largest number of new hypogean taxa were described in the decades of 1940 and especially 1980 (Fig. 1).
The knowledge of the Portuguese stygofauna increased noticeably from the 40's until the 60's, but the greatest expansion was in the 80's with the description of 19 new species (Fig. 1).The researchers of the former Instituto de Investigação "Dr.Augusto Nobre" from Porto University gave the greatest contribution to the description of new species, being only produced out of this institute 11% of this knowledge.José Maria Braga (25 species) and Odette Afonso (21 species) contributed to 74% of the Portuguese stygobiont species (Fig. 2).
The 1940's were the most productive decade of taxonomical studies on the terrestrial hypogean fauna as a re- sult of the great sampling efforts of Barros Machado (Fig. 2), but the activity almost stopped during the 70´s and the 80's.The most important contribution in the past, in number of new troglobiontic taxa was afforded by Vandel, who described 6 species of terrestrial isopods (Vandel 1946) (Fig. 3).Isopods are the most diverse group (Fig. 3) in the Portuguese subterranean fauna, characterized by the absence of hypogean species belonging to groups normally with troglobionts in neighbouring Spain, such as Gastropods, Palpigrads, Diplopods, Leptodirine beetles, and other Arthropod groups.

Fig. 1 -
Fig. 1 -Number of publications and described hypogean taxa per decade until August 2012.