Ronald A. Nussbaum

Predicting distributions of known and unknown reptile species in Madagascar

Despite the importance of tropical biodiversity, informative species distributional data are seldom available for biogeographical study or setting conservation priorities. Modelling ecological niche distributions of species offers a potential soluion; however, the utility of old locality data from museums, and of more recent remotely sensed satellite data, remains poorly explored, especially for rapidly changing tropical landscapes. Using 29 modern data sets of environmental land coverage and 621 chameleon occurrence localities from Madagascar (historical and recent), here we demonstrate a significant ability of our niche models in predicting species distribution. At 11 recently inventoried sites, highest predictive success (85.1%) was obtained for models based only on modern occurrence data (74.7% and 82.8% predictive success, respectively, for pre-1978 and all data combined). Notably, these models also identified three intersecting areas of over-prediction that recently yielded seven chameleon species new to science. We conclude that ecological niche modelling using recent locality records and readily available environmental coverage data provides informative biogeographical data for poorly known tropical landscapes, and offers innovative potential for the discovery of unknown distributional areas and unknown species.

Aligning Conservation Priorities Across Taxa in Madagascar with High-Resolution Planning Tools

Globally, priority areas for biodiversity are relatively well known, yet few detailed plans exist to direct conservation action within them, despite urgent need. Madagascar, like other globally recognized biodiversity hot spots, has complex spatial patterns of endemism that differ among taxonomic groups, creating challenges for the selection of within-country priorities. We show, in an analysis of wide taxonomic and geographic breadth and high spatial resolution, that multitaxonomic rather than single-taxon approaches are critical for identifying areas likely to promote the persistence of most species. Our conservation prioritization, facilitated by newly available techniques, identifies optimal expansion sites for the Madagascar governments current goal of tripling the land area under protection. Our findings further suggest that high-resolution multitaxonomic approaches to prioritization may be necessary to ensure protection for biodiversity in other global hot spots.

Chameleon radiation by oceanic dispersal

Historical biogeography is dominated by vicariance methods that search for a congruent pattern of fragmentation of ancestral distributions produced by shared Earth history. A focus of vicariant studies has been austral area relationships and the break-up of the supercontinent Gondwana. Chameleons are one of the few extant terrestrial vertebrates thought to have biogeographic patterns that are congruent with the Gondwanan break-up of Madagascar and Africa. Here we show, using molecular and morphological evidence for 52 chameleon taxa, support for a phylogeny and area cladogram that does not fit a simple vicariant history. Oceanic dispersal—not Gondwanan break-up—facilitated species radiation, and the most parsimonious biogeographic hypothesis supports a Madagascan origin for chameleons, with multiple ‘out-of-Madagascar’ dispersal events to Africa, the Seychelles, the Comoros archipelago, and possibly Reunion Island. Although dispersal is evident in other Indian Ocean terrestrial animal groups, our study finds substantial out-of-Madagascar species radiation, and further highlights the importance of oceanic dispersal as a potential precursor for speciation.

Extinction vulnerability of tropical montane endemism from warming and upslope displacement: a preliminary appraisal for the highest massif in Madagascar

One of the predicted biological responses to climate warming is the upslope displacement of species distributions. In the tropics, because montane assemblages frequently include local endemics that are distributed close to summits, these species may be especially vulnerable to experiencing complete habitat loss from warming. However, there is currently a dearth of information available for tropical regions. Here, we present a preliminary appraisal of this extinction threat using the herpetological assemblage of the Tsaratanana Massif in northern Madagascar (the islands highest massif), which is rich with montane endemism. We present meteorological evidence (individual and combined regional weather station data and reanalysis forecast data) for recent warming in Madagascar, and show that this trend is consistent with recent climate model simulations. Using standard moist adiabatic lapse rates, these observed meteorological warming trends in northern Madagascar predict upslope species displacement of 17–74 m per decade between 1993 and 2003. Over this same period, we also report preliminary data supporting a trend for upslope distribution movements, based on two surveys we completed at Tsaratanana. For 30 species, representing five families of reptiles and amphibians, we found overall mean shifts in elevational midpoint of 19–51 m upslope (mean lower elevation limit 29–114 m; mean upper elevation limit −8 to 53 m). We also found upslope trends in mean and median elevational observations in seven and six of nine species analysed. Phenological differences between these surveys do not appear to be substantial, but these upslope shifts are consistent with the predictions based on meteorological warming. An elevational range displacement analysis projects complete habitat loss for three species below the 2 °C ‘dangerous’ warming threshold. One of these species is not contracting its distribution, but the other two were not resampled in 2003. A preliminary review of the other massifs in Madagascar indicates potential similar vulnerability to habitat loss and upslope extinction. Consequently, we urgently recommend additional elevational surveys for these and other tropical montane assemblages, which should also include, when possible, the monitoring of local meteorological conditions and habitat change.

A molecular phylogeny of ichthyophiid caecilians (Amphibia: Gymnophiona: Ichthyophiidae): out of India or out of South East Asia?

Recent molecular phylogenetic studies indicate that the rafting Indian plate harboured several isolated vertebrate lineages between ca. 130 and 56 Myr ago that dispersed and diversified ‘out of Indi’ following accretion with Eurasia. A single family of the amphibian order Gymnophiona, the Ichthyophiidae, presently occurs on the Indian plate and across much of South East Asia. Ichthyophiid phylogeny is investigated in order to test competing out of India and out of South East Asia hypotheses for their distribution. Partial sequences of mitochondrial 12S and 16S rRNA and cytochrome b genes for 20 ichthyophiids and proximate outgroups were assembled. Parsimony, maximum–likelihood and distance analyses all recover optimum trees in which uraeotyphlids plus Ichthyophis cf. malabarensis are the sister taxa to all other Ichthyophis, among which the South East Asian taxa are monophyletic. Tree topology and branch lengths indicate that the Indian lineages are more basal and older, and thus are more consistent with the hypothesis that ichthyophiids dispersed from the Indian subcontinent into South East Asia. The estimated relationships also support monophyly of Sri Lankan Ichthyophis, and non–monophyly of striped and unstriped Ichthyophis species groups. Mitochondrial DNA sequences provide evidence that should assist current problematic areas of caecilian taxonomy.

Parental investment by skin feeding in a caecilian amphibian

Although the initial growth and development of most multicellular animals depends on the provision of yolk, there are many varied contrivances by which animals provide additional or alternative investment in their offspring. Providing offspring with additional nutrition should be favoured by natural selection when the consequent increased fitness of the young offsets any corresponding reduction in fecundity. Alternative forms of nutrition may allow parents to delay and potentially redirect their investment. Here we report a remarkable form of parental care and mechanism of parent–offspring nutrient transfer in a caecilian amphibian. Boulengerula taitanus is a direct-developing, oviparous caecilian, the skin of which is transformed in brooding females to provide a rich supply of nutrients for the developing offspring. Young animals are equipped with a specialized dentition, which they use to peel and eat the outer layer of their mothers modified skin. This new form of parental care provides a plausible intermediate stage in the evolution of viviparity in caecilians. At independence, offspring of viviparous and of oviparous dermatotrophic caecilians are relatively large despite being provided with relatively little yolk. The specialized dentition of skin-feeding (dermatophagous) caecilians may constitute a preadaptation to the fetal feeding on the oviduct lining of viviparous caecilians.

Seasonal shifts in clutch size and egg size in the side-blotched lizard, Uta stansburiana Baird and Girard

SummaryThere is evidence that the side-blotched lizard, Uta stansburiana, and some other organisms of temperate latitudes produce fewer and larger eggs as the reproductive season progresses. There are at least two models that could explain this phenomenon.Proponents of the parental investment model claim that females are selected to increase egg size, at the cost of clutch size, late in the season in order to produce larger and competitively superior hatchlings at a time when food for hatchlings is in low supply and when juvenile density is high. In this model the selective agent is relative scarcity of food available to hatchlings late in the reproductive season, and the adaptive response is production of larger offspring.The alternative explanation (bet-hedging model) proposed in this paper is based on the view that the amount of food available to females for the production of late-season clutches is unpredictable, and that selection has favored conservatively small clutches in the late season to insure that each egg is at least minimally provisioned. Smaller clutches, which occur most frequently late in the season, are more likely to consist of larger eggs, compared to larger clutches, for two reasons. Firstly, unlike birds, oviparous lizards cannot alter parental investment after their eggs are deposited, and therefore, in cases of fractional optimal clutch size, the next lower integral clutch size is selected with the remaining reproductive energy allocated to increased egg size. With other factors constant, eggs of smaller clutches will increase more in size than eggs of larger clutches when excess energy is divided among the eggs of a clutch. Secondly, unanticipated energy that may become available for reproduction during energy-rich years will similarly increase egg size a greater amount if divided among fewer eggs.

Caecilian viviparity and amniote origins

A recent evaluation of alternative hypotheses for the origin of the amniotic egg, by mapping a single reproductive-mode character onto a phylogeny of tetrapods, concluded that the alternative hypotheses were equally parsimonious. However, this interpretation is dependent upon a mistaken coding of the caecilian amphibians as showing extended embryo retention. Although some caecilians are viviparous, phylogenetic analyses indicate that oviparity is ancestral for the group. With the coding of caecilians corrected, the most parsimonious inference is that the ancestral amniotes did not practice extended embryo retention. A review of the available data indicates that the widespread view that a majority of caecilians are viviparous is mistaken. Oviparity is the dominant reproductive mode in caecilians as it is in other living amphibians.

On the phylogenetic position of the Uraeotyphlidae

VAN DEVENDER, T. R. 1990. Late Quaternary vegetation and climate of the Sonoran Desert, United States and Mexico, p. 134-165. In: Packrat middens: the last 40,000 years of biotic change. J. L. Betancourt, T. R. van Devender, and P. S. Martin (eds.). Univ. of Arizona Press, Tuscon. VANICEK, C. D., AND D. R. FRANKLIN. 1970. Distribution of Green River fishes in Utah and Colorado following closure of Flaming Gorge Dam. Southwestern Nat. 14:297-315. WEIR, B. 1990. Genetic data analysis. Sinauer Associates, Sunderland, MA. WINOGRAD, I. J., J. B. COPLEN, J. M. LANDWEHR, A. C. RIGGS, K. R. LUDWIG, B.J. SZABO, P. T. KOLESAR, AND K. M. REVESZ. 1992. Continuous 500,000-year climate record from vein calcite in Devils Hole, Nevada. Science 258:255-260.

Life-history evolution and mitogenomic phylogeny of caecilian amphibians

We analyze mitochondrial genomes to reconstruct a robust phylogenetic framework for caecilian amphibians and use this to investigate life-history evolution within the group. Our study comprises 45 caecilian mitochondrial genomes (19 of them newly reported), representing all families and 27 of 32 currently recognized genera, including some for which molecular data had never been reported. Support for all relationships in the inferred phylogenetic tree is high to maximal, and topology tests reject all investigated alternatives, indicating an exceptionally robust molecular phylogenetic framework of caecilian evolution consistent with current morphology-based supraspecific classification. We used the mitogenomic phylogenetic framework to infer ancestral character states and to assess correlation among three life-history traits (free-living larvae, viviparity, specialized pre-adult or vernal teeth), each of which occurs only in some caecilian species. Our results provide evidence that an ancestor of the Seychelles caecilians abandoned direct development and re-evolved a free-living larval stage. This study yields insights into the concurrent evolution of direct development and of vernal teeth in an ancestor of Teresomata that likely gave rise to skin-feeding (maternal dermatophagy) behavior and subsequently enabled evolution of viviparity, with skin feeding possibly a homologous precursor of oviduct feeding in viviparous caecilians.