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Diversity of Arthropods Preyed Upon by the CarnivorousPlant Pinguicula moranensis (Lentibulariaceae) in aTemperate Forest of Central MexicoAuthor(s): Numa P. Pavón, Atilano Contreras-Ramos, and Yadira Islas-PerusquíaSource: The Southwestern Naturalist, 56(1):78-82. 2011.Published By: Southwestern Association of NaturalistsDOI: http://dx.doi.org/10.1894/JC-36.1URL: http://www.bioone.org/doi/full/10.1894/JC-36.1

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DIVERSITY OF ARTHROPODS PREYED UPON BY THE CARNIVOROUS PLANTPINGUICULA MORANENSIS (LENTIBULARIACEAE) IN A TEMPERATE FOREST

OF CENTRAL MEXICO

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 Biologıa, Departamento de Zoologıa, Universidad Nacional Autonoma de Mexico, Apartado Postal 70-153,

04510 Mexico, Distrito Federal, Mexico (ACR)

*Correspondent: acontreras@ibiologia.unam.mx

ABSTRACT—Diversity of arthropods preyed upon by the carnivorous plant Pinguicula moranensis wasanalyzed during 2006 within a pine-oak (Pinus-Quercus) forest in the Sierra de Pachuca, Hidalgo,Mexico. A total of 570 individuals of nine orders was collected. Hemiptera was recorded as prey of thisplant for the first time. The most prevalent order was Diptera, with 53.6% of total prey; within this order,Sciaridae accounted for 64.7% of prey. The month with the highest values for alpha diversity was July (H5 1.32). Greatest turnover of orders was June–November and that of families of Diptera was July–August. Total beta diversity was greater in families of Diptera, with a value of 1.29, while that of orders ofarthropods was 0.53.

RESUMEN—Se analizo la diversidad de presas de artropodos en la planta carnıvora Pinguiculamoranensis durante 2006 en un bosque de pino-encino (Pinus-Quercus) en la Sierra de Pachuca, Hidalgo,Mexico. Se recolecto un total de 570 individuos de nueve ordenes. Hemiptera no se tenıa registradoanteriormente como presa de esta planta. El orden de mayor importancia fue Diptera, con 53.6% deltotal de presas; dentro de este orden, Sciaridae contribuyo con 64.7% de las presas. El mes con losvalores mas altos de diversidad alfa fue julio (H 5 1.32). El recambio mas alto de ordenes fue entrejunio y noviembre y el de familias de Diptera fue entre julio y agosto. La diversidad beta total fue masalta en las familias de Diptera, con un valor de 1.29, mientras que la de los ordenes de artropodos tuvoun valor de 0.53.

The immediate benefit of a carnivorous habit inplants is a significant increase in rate of photosyn-thesis derived from a higher concentration ofnutrients in leaves (Aldenius et al., 1983; Wake-field et al., 2005; Ellison, 2006). Plants obtainnitrogen, phosphorus, potassium, and magnesiumfrom captured prey; nonetheless, ca. 60% ofnitrogen is sequestered by bacteria (Karlsson andCarlsson, 1984; Adamec, 2002; Farnsworth andEllison, 2008). Incorporation of nutrients comingfrom prey allows plants to assign resources to rootsfor uptake of nitrogen (Karlsson and Carlsson,1984; Adamec, 2002). In this way, economy ofnutrients in carnivorous plants, expressed in termsof efficiencies of use of photosynthetic nutrients, isclosely linked to capture of prey. This resolvesdeficiencies of nutrients that generally character-ize the substrate where the plant grows (Farns-worth and Ellison, 2008).

Presence of potential animal prey for carniv-orous plants may vary among environments andseasons, so that different populations of plantsestablish themselves in the presence of particularcommunities of prey (Zamora et al., 1998; Alcalaand Domınguez, 2003). Capture of prey normal-ly is lower than availability of prey (Harms, 1999;Jobson and Morris, 2001). Also, there is a highsuccess in escaping from the traps, whichdepends mainly on size of insects (Gibson,1991).

Carnivorous plants are generalists, with a dietthat includes diverse animals such as insects,arachnids, gastropods, and other arthropods(Alcala and Domınguez, 2003). In Sarraceniapurpurea, Hymenoptera (Formicidae), Coleop-tera, and Gastropoda constitute 69% of totalmass of prey. In the aquatic carnivorous plantUtricularia, small organisms such as rotifers,

THE SOUTHWESTERN NATURALIST 56(1):78–82 MARCH 2011

cladocerans, copepods, annelids, rhizopodans,and phytoplankton (Bacillariophyta, Chloro-phyta, Cyanophyta, and Euglenophyta), as wellas insects, have been recorded as captured(Gordon and Pacheco, 2007). Diet of Pinguiculaconsists mainly of insects 1–4 mm long, mostlyflying insects with Diptera contributing ca. 80%of captures (Antor and Garcıa, 1994; Alcala andDomınguez, 2003). As an example, diet ofPinguicula vulgaris, which inhabits northernSweden, consists solely of black flies (Diptera:Simuliidae; Adler and Malmqvist, 2004). Thispattern might be a consequence of mechanismsthat attract prey, i.e., reflection of ultravioletlight by mucilage on leaves of the summerrosette of Pinguicula (Joel et al., 1985; Antorand Garcıa, 1994; Adler and Malmqvist, 2004).

Most studies of diet of carnivorous plantsidentify prey to taxonomic order. Nonetheless,to determine the feeding ecology of carnivorousplants, a more precise taxonomic effort isnecessary to quantify the relative proportion oftaxa that are being trapped by these plants(Givnish, 1989), as well as to elucidate seasonalvariation in captures (Karlsson et al., 1994;Jobson and Morris, 2001). The main goal ofour study was to describe temporal beta diversityof prey of Pinguicula moranensis in a temperateforest of central Mexico. Also, our study attempt-ed to describe temporal variation in diversity ofinsects. Abundance of insects might be a limitingfactor for growth of this generalist plant, sofluctuations in prey might help better under-stand dynamics of this carnivorous species.

MATERIALS AND METHODS—Pinguicula moranensis is themost common and widespread species of this genus inMexico. This is a perennial herb with basal leavesforming a rosette, which varies seasonally: winterrosette, with spatulate to lanceolate leaves, up to 4 cmlong and 1.5 cm wide; summer rosette, with obovate tonearly circular leaves, up to 10 cm long and 7 cm wide,with glandular hairs on the upper side that secrete adigestive mucilage that makes the leaves sticky (deRzedowski and Rzedowski, 2001).

Our work was performed on a population of P.moranensis within a pine-oak (Pinus-Quercus) forest inthe Sierra de Pachuca, which is part of the Sierra MadreOriental, within the state of Hidalgo in central Mexico(2,420 m above sea level; 20u069–20u099N, 98u309–98u329W). Climate of the study site was temperatesubhumid 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 EnvironmentalManagement Unit or Unidad de Manejo Ambientalbefore the Ministry of the Environment of the Mexicangovernment (SEMARNAT-UMA-EX -0027- HGO). Be-

sides exploitation of forests, which has occurred duringthe past 20 years, the site is in a program ofconservation, research, ecotourism, and environmentaleducation (Chavez-Peon, 2005).

In January 2006, 25 plants were randomly selectedfrom a total of 48 individuals at the study site. DuringJanuary–May 2006, plants maintained their winterrosette and remained hidden in the soil, so only thoseflowering were visible. During June–November 2006,when plants had the summer or functional rosette,prey stuck to leaves of marked plants were collectedmonthly (except October). Prey items were preservedin 70% ethanol. Specimens were identified to orderand, for Diptera, to family through keys in Borror andWhite (1970), McAlpine et al. (1981), and Triplehornand Johnson (2004).

Species richness, Shannon’s index, and equitability(Moreno, 2001) were calculated for each month duringwhich plants bore summer rosettes (June–November).Estimations were performed considering data fororders and for families of Diptera separately. Also, ab-diversity value was calculated for each pair of months,and a temporal btotal-value was obtained using theWilson-Shmida index (Moreno, 2001). These estima-tions were calculated with the program SpeciesDiversity and Richness (Henderson and Seaby, 2002).

RESULTS—Plants in the population of P. mor-anensis had a functional prey-capturing rosettefrom mid-May through mid-November. Duringthis period, 570 individuals of nine orders werecollected from marked plants, seven of whichbelonged to the class Insecta (Table 1). Themost commonly trapped order was Diptera,which contributed 53.6% of prey. Within Dip-tera, Sciaridae was the family with most individ-uals captured with 64.7% of the total (Table 1).

Highest values for richness of orders andShannon’s diversity were during July (Table 2).Highest richness for diversity of families ofDiptera was in August; nonetheless, equitabilitywas low. This is due to the increase of Sciaridae,with 67.5% of total prey. The most importantturnover of orders occurred June–November, asa consequence of a missing representation ofHemiptera and Lepidoptera during July (Ta-ble 3). The highest value of Wilson and Schmi-da’s index for Diptera was July–August (Table 3).This was due to the appearance in August of preyin the families Anisopodidae, Culicidae, Myceto-philidae, and Psychodidae, as well as the absenceof Empididae and Ceratopogonidae. Total betadiversity was higher for families of Diptera, with avalue of 1.29, than for orders, which had a lowervalue of 0.53.

DISCUSSION—The number of orders recordedin our study is similar to those from studies on

March 2011 Pavon et al.—Prey of carnivorous plants 79

species of Pinguicula, particularly to those on P.moranensis (Aldenius et al., 1983; Antor andGarcıa, 1994; Karlsson et al., 1994; Alcala andDomınguez, 2003). In our study, individuals ofHemiptera, not recorded previously as prey ofPinguicula, are reported. Nonetheless, numbers

of prey of this order were scarce; for instance,only one homopteran was found attached to aleaf in July. In previous studies of diversity ofarthropods in litter at the same study site, 28orders of invertebrates were recorded, includingall orders trapped by P. moranensis (Chavez-Peon,2005; Martınez-Falcon, 2006). Larger individualsfrom the remaining orders inhabiting litter onthe study site (e.g., Pseudoscorpionida, Blatto-dea, Opilionida, and Julida) are less likely to betrapped by leaves of the carnivorous plants,because they might have a better chance ofescaping (Gibson, 1991).

The arthropod order that contributed thegreatest number of prey was Diptera, which isconcordant with other research on the diet ofPinguicula. However, the percentage recorded inour study (53.6%) is lower than that reported forthe diet of Pinguicula in other environments,which was 55–99% (Alcala and Domınguez,2003; Adler and Malmqvist, 2004). This differ-ence is due to the contribution of other groupsthat might be abundant in the surroundinghabitat, as was the case of Collembola, whichdominated in litter at our study site. Meanwhile,in habitats with a poor representation of otherorders of arthropods, the contribution of Dip-tera increases. In a population of P. vulgaris neara lake in Sweden where simuliid black flies wereabundant, dipterans represented 85% of the 915captured arthropods; among these, Cnephiaeremites and Cnephia pallipes accounted for.97% of the total number of blackflies (Adlerand Malmqvist, 2004). The pattern of greaterincidence of dipteran prey may be expectedbecause leaves of Pinguicula might have reflec-tion of ultraviolet light as a special attractant(Antor and Garcıa, 1994; Adler and Malmqvist,2004). Based on this reflection of ultraviolet lightas an attractant, it appears that feeding behavior

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

TaxaDiversity

parameters June July August September November

Orders Richness 6 8 7 7 5Shannon index 0.8 1.32 0.99 1.18 1.19Evenness 0.45 0.63 0.51 0.6 0.74

Families ofDiptera

Richness 5 6 8 5 3Shannon index 1.02 1.48 1.1 1.15 0.7Evenness 0.63 0.82 0.53 0.71 0.63

TABLE 1—Orders of insects and arachnids andfamilies of Diptera collected from leaves of Pinguiculamoranensis in a pine-oak (Pinus-Quercus) forest inHidalgo, Mexico. Percentage of each order wascalculated based on total number of individualscaptured during 2006; percentage of each family ofDiptera was calculated based on total number ofindividuals of Diptera captured during 2006.

Taxon Percentage of total

Insecta

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

Arachnida

Acari 11.6Araneae 1.6

Families of Diptera

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

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of P. moranensis tends toward a specialization ondipterans. If true, there would be a significanttemporal limitation of the resource becausedipterans are abundant only in June and August.Through the rest of the growth period, plantscapture prey of other taxa that, perhaps bychance, contact the leaves and are digested. Thisgenerates, overall, a broader range of kinds ofprey during the growth period, so that the plantshould still be considered a generalist.

Most previous studies on this generalist car-nivorous plants analyzed prey at the ordinallevel. Our study considered dipteran prey at thefamily level, showing that finer taxonomicanalysis might produce a better understandingof patterns of consumption of prey by this plant.

We thank R. Campuzano and C. Chavez-Peon for theopportunity to conduct this study on their property.This study was funded by Universidad Autonoma delEstado de Hidalgo through Programa Anual deInvestigacion 2007. Support from Instituto de Biologıaof Universidad Nacional Autonoma de Mexico to ACR,for establishment of this collaboration, is gratefullyacknowledged.

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

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Submitted 3 April 2009. Accepted 3 May 2010.Associate Editor was Jerry L. Cook.

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