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Diversity of arthropods preyed upon by the carnivorous plant Pinguicula moranensis (Lentibulariaceae) in a temperate forest of central Mexico.

The immediate benefit of a carnivorous habit in plants is a significant increase in rate of photosynthesis derived from a higher concentration of nutrients in leaves (Aldenius et al., 1983; Wakefield et al., 2005; Ellison, 2006). Plants obtain nitrogen, phosphorus, potassium, and magnesium from captured prey; nonetheless, ca. 60% of nitrogen is sequestered by bacteria (Karlsson and Carlsson, 1984; Adamec, 2002; Farnsworth and Ellison, 2008). Incorporation of nutrients coming from prey allows plants to assign resources to roots for uptake of nitrogen (Karlsson and Carlsson, 1984; Adamec, 2002). In this way, economy of nutrients in carnivorous plants, expressed in terms ofefficiencies of use of photosynthetic nutrients, is closely linked to capture of prey. This resolves deficiencies of nutrients that generally characterize the substrate where the plant grows (Farnsworth and Ellison, 2008).

Presence of potential animal prey for carnivorous plants may vary among environments and seasons, so that different populations of plants establish themselves in the presence of particular communities of prey (Zamora et al., 1998; Alcala and Dominguez, 2003). Capture of prey normally is lower than availability of prey (Harms, 1999; Jobson and Morris, 2001). Also, there is a high success in escaping from the traps, which depends mainly on size of insects (Gibson, 1991).

Carnivorous plants are generalists, with a diet that includes diverse animals such as insects, arachnids, gastropods, and other arthropods (Alcala and Dominguez, 2003). In Sarracenia purpurea, Hymenoptera (Formicidae), Coleoptera, and Gastropoda constitute 69% of total mass of prey. In the aquatic carnivorous plant Utricularia, small organisms such as rotifers, cladocerans, copepods, annelids, rhizopodans, and phytoplankton (Bacillariophyta, Chlorophyta, Cyanophyta, and Euglenophyta), as well as insects, have been recorded as captured (Gordon and Pacheco, 2007). Diet of Pinguicula consists mainly of insects 1-4 mm long, mostly flying insects with Diptera contributing ca. 80% of captures (Antor and Garcia, 1994; Alcala and Dominguez, 2003). As an example, diet of Pinguicula vulgaris, which inhabits northern sweden, consists solely of black flies (Diptera: Simuliidae; Adler and Malmqvist, 2004). This pattern might be a consequence of mechanisms that attract prey, i.e., reflection of ultraviolet light by mucilage on leaves of the summer rosette of Pinguicula (Joel et al., 1985; Antor and Garcia, 1994; Adler and Malmqvist, 2004).

Most studies of diet of carnivorous plants identify prey to taxonomic order. Nonetheless, to determine the feeding ecology of carnivorous plants, a more precise taxonomic effort is necessary to quantify the relative proportion of taxa that are being trapped by these plants (Givnish, 1989), as well as to elucidate seasonal variation in captures (Karlsson et al., 1994; Jobson and Morris, 2001). The main goal of our study was to describe temporal beta diversity of prey of Pinguicula moranensis in a temperate forest of central Mexico. Also, our study attempted to describe temporal variation in diversity of insects. Abundance of insects might be a limiting factor for growth of this generalist plant, so fluctuations in prey might help better understand dynamics of this carnivorous species.

MATERIALS AND METHODS--Pinguicula moranensis is the most common and widespread species of this genus in Mexico. This is a perennial herb with basal leaves forming a rosette, which varies seasonally: winter rosette, with spatulate to lanceolate leaves, up to 4 cm long and 1.5 cm wide; summer rosette, with obovate to nearly circular leaves, up to 10 cm long and 7 cm wide, with glandular hairs on the upper side that secrete a digestive mucilage that makes the leaves sticky (de Rzedowski and Rzedowski, 2001).

Our work was performed on a population of P. moranensis within a pine-oak (Pinus-Quercus) forest in the Sierra de Pachuca, which is part of the Sierra Madre Oriental, within the state of Hidalgo in central Mexico (2,420 m above sea level; 20[degrees]06'-20[degrees]09'N, 98[degrees]30'98[degrees]32'W). Climate of the study site was temperate subhumid with a cold winter and rain during summer; range of annual precipitation was 1,500-2,000 mm. The study site is registered as an Environmental Management Unit or Unidad de Manejo Ambiental before the Ministry of the Environment of the Mexican government (SEMARNAT-UMA-EX -0027- HGO). Besides exploitation of forests, which has occurred during the past 20 years, the site is in a program of conservation, research, ecotourism, and environmental education (Chavez-Peon, 2005).

In January 2006, 25 plants were randomly selected from a total of 48 individuals at the study site. During January-May 2006, plants maintained their winter rosette and remained hidden in the soil, so only those flowering were visible. During June-November 2006, when plants had the summer or functional rosette, prey stuck to leaves of marked plants were collected monthly (except october). Prey items were preserved in 70% ethanol. specimens were identified to order and, for Diptera, to family through keys in Borror and White (1970), McAlpine et al. (1981), and Triplehorn

and Johnson (2004).

Species richness, Shannon's index, and equitability (Moreno, 2001) were calculated for each month during which plants bore summer rosettes (June-November). Estimations were performed considering data for orders and for families of Diptera separately. Also, a b-diversity value was calculated for each pair of months, and a temporal [[beta].sub.total-]value was obtained using the Wilson-Shmida index (Moreno, 2001). These estimations were calculated with the program species Diversity and Richness (Henderson and Seaby, 2002).

RESULTS--Plants in the population of P. moranensis had a functional prey-capturing rosette from mid-May through mid-November. During this period, 570 individuals of nine orders were collected from marked plants, seven of which belonged to the class Insecta (Table 1). The most commonly trapped order was Diptera, which contributed 53.6% of prey. Within Diptera, Sciaridae was the family with most individuals captured with 64.7% of the total (Table 1).

Highest values for richness of orders and Shannon's diversity were during July (Table 2). Highest richness for diversity of families of Diptera was in August; nonetheless, equitability was low. This is due to the increase of Sciaridae, with 67.5% of total prey. The most important turnover of orders occurred June-November, as a consequence of a missing representation of Hemiptera and Lepidoptera during July (Table 3). The highest value of Wilson and Schmida's index for Diptera was July-August (Table 3). This was due to the appearance in August of prey in the families Anisopodidae, Culicidae, Mycetophilidae, and Psychodidae, as well as the absence of Empididae and Ceratopogonidae. Total beta diversity was higher for families of Diptera, with a value of 1.29, than for orders, which had a lower value of 0.53.

DISCUSSION--The number of orders recorded in our study is similar to those from studies on species of Pinguicula, particularly to those on P. moranensis (Aldenius et al., 1983; Antor and Garcia, 1994; Karlsson et al., 1994; Alcala and Dominguez, 2003). In our study, individuals of Hemiptera, not recorded previously as prey of Pinguicula, are reported. Nonetheless, numbers of prey of this order were scarce; for instance, only one homopteran was found attached to a leaf in July. In previous studies of diversity of arthropods in litter at the same study site, 28 orders of invertebrates were recorded, including all orders trapped by P. moranensis (Chavez-Peon, 2005; Martinez-Falcon, 2006). Larger individuals from the remaining orders inhabiting litter on the study site (e.g., Pseudoscorpionida, Blattodea, opilionida, and Julida) are less likely to be trapped by leaves of the carnivorous plants, because they might have a better chance of escaping (Gibson, 1991).

The arthropod order that contributed the greatest number of prey was Diptera, which is concordant with other research on the diet of Pinguicula. However, the percentage recorded in our study (53.6%) is lower than that reported for the diet of Pinguicula in other environments, which was 55-99% (Alcala and Dominguez, 2003; Adler and Malmqvist, 2004). This difference is due to the contribution of other groups that might be abundant in the surrounding habitat, as was the case of Collembola, which dominated in litter at our study site. Meanwhile, in habitats with a poor representation of other orders of arthropods, the contribution of Diptera increases. In a population of P. vulgaris near a lake in Sweden where simuliid black flies were abundant, dipterans represented 85% of the 915 captured arthropods; among these, Cnephia eremites and Cnephia pallipes accounted for >97% of the total number of blackflies (Adler and Malmqvist, 2004). The pattern of greater incidence of dipteran prey may be expected because leaves of Pinguicula might have reflection of ultraviolet light as a special attractant (Antor and Garcia, 1994; Adler and Malmqvist, 2004). Based on this reflection ofultraviolet light as an attractant, it appears that feeding behavior of P. moranensis tends toward a specialization on dipterans. If true, there would be a significant temporal limitation of the resource because dipterans are abundant only in June and August. Through the rest of the growth period, plants capture prey of other taxa that, perhaps by chance, contact the leaves and are digested. This generates, overall, a broader range of kinds of prey during the growth period, so that the plant should still be considered a generalist.

Most previous studies on this generalist carnivorous plants analyzed prey at the ordinal level. our study considered dipteran prey at the family level, showing that finer taxonomic analysis might produce a better understanding of patterns of consumption of prey by this plant.

We thank R. Campuzano and C. Chavez-Peon for the opportunity to conduct this study on their property. This study was funded by Universidad Autonoma del Estado de Hidalgo through Programa Anual de Investigacion 2007. Support from Instituto de Biologia of Universidad Nacional Autonoma de Mexico to ACR, for establishment of this collaboration, is gratefully acknowledged.

Associate Editor was Jerry L. Cook.

Submitted 3 April 2009. Accepted 3 May 2010.

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* Correspondent: acontreras@ibiologia.unam.mx

NUMA P. PAVON, ATILANO CONTRERAS-RAMOS, * and YADIRA ISLAS-PERUSQUIA

Centro de Investigaciones Biologicas, Universidad Autonoma del Estado de Hidalgo, Apartado Postal 1-69, Pachuca, Hidalgo 42001, Mexico (NPP, YIP)

Instituto de Biologia, Departamento de Zoologia, Universidad Nacional Autonoma de Mexico, Apartado Postal 70-153, 04510 Mexico, Distrito Federal, Mexico (ACR)
Table 1--Orders of insects and arachnids and
families of Diptera collected from leaves of Pinguicula
moranensis in a pine-oak (Pinus-Quercus) forest in
Hidalgo, Mexico. Percentage of each order was
calculated based on total number of individuals
captured during 2006; percentage of each family of
Diptera was calculated based on total number of
individuals of Diptera captured during 2006.

Taxon                 Percentage of total

Insecta

Collembola                           29.1
Hemiptera                             0.9
Coleoptera                            0.5
Diptera                              53.6
Hymenoptera                           1.8
Lepidoptera                           0.2
Psocoptera                            0.7

Arachnida

Acari                                11.6
Araneae                               1.6

Families of Diptera

Anisopodidae                          1.0
Bibionidae                            0.5
Cecidomyiidae                        16.2
Ceratopogonidae                       0.5
Chironomidae                          7.8
Culicidae                             0.5
Empididae                             0.5
Mycetophilidae                        1.5
Phoridae                              6.4
Psychodidae                           0.5
sciaridae                            64.7

Table 2--Alpha-diversity values calculated for months when
Pinguicula moranensis displayed functional rosettes
for capturing arthropod prey in Hidalgo, Mexico. Estimations
were made for orders of insects and arachnids and
for families of Diptera.

              Diversity
Taxa          parameters      June   July   August

Orders        Richness           6      8        7
              Shannon index    0.8   1.32     0.99
              Evenness        0.45   0.63     0.51
Families of   Richness           5      6        8
Diptera       Shannon index   1.02   1.48      1.1
              Evenness        0.63   0.82     0.53

              Diversity
Taxa          parameters      September   November

Orders        Richness                7          5
              Shannon index        1.18       1.19
              Evenness              0.6       0.74
Families of   Richness                5          3
Diptera       Shannon index        1.15        0.7
              Evenness             0.71       0.63

Table 3--Beta-diversity values of Wilson and Shmida estimating
turnover of orders (below diagonal) and families of Diptera
(above diagonal) among sampling months during a study of prey
captured by Pinguicula moranensis in Hidalgo, Mexico.

Month       June   July   August   September   November

June          --   0.27     0.38        0.56       0.86
July        0.28     --     0.97        0.27       0.56
August      0.38   0.06       --        0.23       0.45
September   0.38   0.06     0.00          --       0.50
November    0.45   0.23     0.16        0.16         --
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Author:Pavon, Numa P.; Contreras-Ramos, Atilano; Islas-Perusquia, Yadira
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1MEX
Date:Mar 1, 2011
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