Invasion biology in non-free-living species: interactions between abiotic (climatic) and biotic (host availability) factors in geographical space in crayfish commensals (Ostracoda, Entocytheridae)

Abstract

In invasion processes, both abiotic and biotic factors are considered essential, but the latter are usually disregarded when modeling the potential spread of exotic species. In the framework of set theory, interactions between biotic (B), abiotic (A), and movement-related (M) factors in the geographical space can be hypothesized with BAM diagrams and tested using ecological niche models (ENMs) to estimate A and B areas. The main aim of our survey was to evaluate the interactions between abiotic (climatic) and biotic (host availability) factors in geographical space for exotic symbionts (i.e., non-free-living species), using ENM techniques combined with a BAM framework and using exotic Entocytheridae (Ostracoda) found in Europe as model organisms. We carried out an extensive survey to evaluate the distribution of entocytherids hosted by crayfish in Europe by checking 94 European localities and 12 crayfish species. Both exotic entocytherid species found, Ankylocythere sinuosa and Uncinocythere occidentalis, were widely distributed in W Europe living on the exotic crayfish species Procambarus clarkii and Pacifastacus leniusculus, respectively. No entocytherids were observed in the remaining crayfish species. The suitable area for A. sinuosa was mainly restricted by its own limitations to minimum temperatures in W and N Europe and precipitation seasonality in circum-Mediterranean areas. Uncinocythere occidentalis was mostly restricted by host availability in circum-Mediterranean regions due to limitations of P. leniusculus to higher precipitation seasonality and maximum temperatures. The combination of ENMs with set theory allows studying the invasive biology of symbionts and provides clues about biogeographic barriers due to abiotic or biotic factors limiting the expansion of the symbiont in different regions of the invasive range. The relative importance of abiotic and biotic factors on geographical space can then be assessed and applied in conservation plans. This approach can also be implemented in other systems where the target species is closely interacting with other taxa.

Keywords: BAM diagrams; Biological invasions; ecological niche models; host availability.

Figure 1

BAM diagrams adapted from Jiménez-Valverde et al. (2011) representing the three possible interactions between environmental and biotic factors in the geographical space of a species distribution model for invasive species when the species has no dispersal limitations ((A ∪ B) ⊂ M). Represented by circles, A is the geographical area with suitable environmental conditions, B the area where biotic interactions allow species existence, and M is the accessible area for the species. G_BI is the available geographical area with favorable environmental conditions, but inappropriate biotic conditions (G_BI = A\B) and BI the area with unsuitable environmental, but appropriate biotic conditions (BI = B\A) for the species. Within this model frame, the three possible interactions between A and B are as follows: (A) A includes B (B ⊂ A or (A\B ≠ ∅) ∧ (B\A = ∅)), (B) B includes A (A ⊂ B or (A\B = ∅) ∧ (B\A ≠ ∅)), and (C) a partial overlap between A and B ((A\B ≠ ∅) ∧ (B\A ≠ ∅)). Colors for G_BI and BI as in Fig. 5.

Figure 2

(A–C) Scanning electron microscope (SEM) and (D) stereomicroscope photographs of Uncinocythere occidentalis specimens from (A–C) LOC047 and (D) LOC039 (for information about locality codes, see Table S1 in Supporting Information). (A) Mating pair of an adult male (top) and an A-1 female (bottom); (B,C) copulatory organs of adult males in (B) lateral and (C) sublateral views; (D) mating pair of an adult male (top) and an A-2 female (bottom). A-1 refers to the last developmental instar prior to the adult, and A-2 to the juvenile instar prior to A-1.

Figure 3

(A,B) Consensus projections obtained from combining the 800 ecological niche models for (A) Ankylocythere sinuosa and (B) Procambarus clarkii using ensemble modeling techniques, showing the potential climatic suitability for both species in Europe (12°W–60°E; 30°N–75°N). (C,D) Variability among the 100 ensemble projections used to build the consensus projection for (C) Ankylocythere sinuosa and (D) Procambarus clarkii. Black dots in (C) are localities with A. sinuosa occurrences from our field survey. The maps have a 5-arcmin resolution and a Mollweide equal-area projection.

Figure 4

(A,B) Consensus projections obtained from combining the 800 ecological niche models for (A) Uncinocythere occidentalis and (B) Pacifastacus leniusculus using ensemble modeling techniques, showing the potential climatic suitability for both species in Europe (12°W–60°E; 30°N–75°N). (C,D) Variability among the ensemble projections used to build the consensus projection for (C) Uncinocythere occidentalis and (D) Pacifastacus leniusculus. Black dots in (C) are localities with U. occidentalis occurrences from our field survey. The maps have a 5-arcmin resolution and a Mollweide equal-area projection.

Figure 5

Combined entocytherid-host binary transformed consensus projections for species pairs (A) Ankylocythere sinuosa and Procambarus clarkii, (B) Uncinocythere occidentalis and Pacifastacus leniusculus, showing those areas climatically suitable for the symbiont but unsuitable for its host (G_BI), and the climatically unsuitable areas for the symbiont and suitable for the host (BI), in Europe (12°W–60°E; 30°N–75°N). The maps have a 5-arcmin resolution and a Mollweide equal-area projection (see Fig. 1 and text for definitions of the G_BI and BI areas; colors for G_BI and BI as in Fig. 1).