Interciencia ISSN: 0378-1844 [email protected] Asociación Interciencia

Ramos-Zapata, José A.; Orellana, Roger; Allen, Edith B. Mycorrhizal dynamics and dependence of orthacanthos martius (), a native palm of the Yucatan Peninsula, Mexico Interciencia, vol. 31, núm. 5, mayo, 2006, pp. 364-370 Asociación Interciencia Caracas, Venezuela

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How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the , Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative MYCORRHIZAL DYNAMICS AND DEPENDENCE OF MARTIUS (ARECACEAE), A NATIVE PALM OF THE YUCATAN PENINSULA, MEXICO

José A. Ramos-Zapata, Roger Orellana and Edith B. Allen

SUMMARY

Field observations were carried out to determine the seasonal sites during the wet season, but was equally high during one dry patterns and recovery from disturbance by arbuscular mycorrhizal season observation in the abandoned milpa. Spore density was (AM) associations in Desmoncus orthacanthos Martius, eight years highest during the dry season. The RMD ranged from 7.8 to following shifting agriculture and in a mature forest. In addition, 54.9%, with greater biomass of mycorrhizal than non-mycorrhizal a greenhouse experiment was performed to determine the relative using P solutions that mimicked field soil concentrations. mycorrhizal dependency (RMD) of this species. Four growth This suggests that this slow-growing palm is highly dependent on stages were selected, and roots and rhizosphere soil of five indi- mycorrhizal fungi in local soils and maintains relatively high AM viduals from each stage were monitored during one year. A sea- activity even during the dry season. Culture of this slow-growing, sonal pattern, but no difference in abandoned agriculture and ma- understory palm for the rattan industry requires that soils be man- ture forest were found in AM fungal activity. Soil moisture, spores aged for high levels of AM fungi. The study showed that the stan- per gram of soil, and percentage of root colonization were not dard local practice of shifting agriculture enables sufficient recov- correlated during this year. Root colonization was highest at both ery of soil inoculum for growth of D. orthacanthos.

RESUMEN

Se realizaron observaciones en una parcela (milpa) abandona- je de colonización fue mayor en ambos sitios durante la etapa da de ocho años de edad y en una selva madura para determi- de lluvias, este porcentaje fue igual de elevado en una tempora- nar la dinámica estacional y la recuperación de una perturba- da de secas en la milpa abandonada. La densidad de esporas ción en la asociación micorrícica arbuscular (MA) presente en fue mayor en la temporada de secas. Los valores calculados de Desmoncus orthacanthos Martius. En una prueba de invernadero RMD se encuentran entre 7.8 y 54.9%, con una mayor biomasa se evaluó la dependencia micorrícica relativa (RMD) de esta es- en las plantas micorrizadas comparadas con las no-micorrizadas pecie. En el campo se seleccionaron cuatro etapas de crecimien- usando concentraciones de fósforo similares a las presentes en to en esta palmera y se monitoreó durante un año las raíces y el el suelo de los sitios de estudio. Los resultados sugieren que suelo rizosférico de cinco individuos de cada etapa de creci- esta especie es dependiente de la asociación micorrícica en las miento. Se detectó una dinámica estacional, pero no diferencia condiciones evaluadas y mantiene una actividad de AM relativa- en la actividad de la asociación comparando la milpa abando- mente alta incluso durante la temporada de secas. Los resulta- nada y la selva madura. No se encontró correlación, durante el dos sugieren que las practicas agrícolas empleadas en la zona período de estudio, entre la humedad del suelo, densidad de es- de estudio permiten la recuperación del potencial de inoculo del poras por gramo de suelo y colonización de raíces. El porcenta- suelo para el crecimiento de D. orthacanthos.

Introduction uptake and resistance to water can explore and capture nutri- mass (Pankow et al., 1991; stress (Ruiz-Lozano et al., ents from a larger volume of Johnson and Wedin, 1997). The role of the arbuscular 1995; Augé, 2001; Querejeta soil compared to non-mycor- In tropical forests where mycorrhizal (AM) association et al., 2003), and increased rhizal roots (Attiwill and competition for light, nutri- in improving the growth of nutrient uptake (especially P Adams, 1993; Bhatia et al., ents and water may be high, individual plants has been ex- and N; Marschner and Dell, 1996). the AM association can influ- tensively investigated. This 1994; Siqueira and Saggin- Mature tropical ecosystems ence the ability of plants to association offers the host Junior, 2001). The mycor- are characterized by con- acquire nutrients and increase protection against soil rhizal association is important tinual, year-long nutrient cy- plant growth and fitness pathogens (Azcón-Aguilar and for nutrient cycling since cling for the incorporation of (Zobel et al., 1997; Allen et Barea, 1996), improved water roots with external hyphae mineral resources into bio- al., 2003). In spite of the im-

KEYWORDS / Arbuscular Mycorrhiza / Dependency / Seasonal Patterns / Understory Palms / Received: 08/15/2005 Modified: 03/01/2006 Accepted: 03/08/2006. José A. Ramos-Zapata. Biologist, Researcher, Universidad Autó- tad de Ciencias, UNAM, Edith B. Allen. Biologist, Tufts Universidad Autónoma de noma de Yucatán. A.P. 4-116, México. PhD Ecology, Facul- University, MA, USA. MSc Yucatán, Mexico. MS Environ- Itzimná, C.P. 97000. Mérida, tad de Ciencias Biológicas, Botany Rutgers University, mental Microbiology, Univer- Yucatán, Mexico. e-mail: Universidad de Sevilla, Spain. N.J., USA. PhD Botany, Uni- sity of Aberdeen, UK. PhD [email protected] Researcher. Centro de Investi- versity of Wyoming, USA. Biotechnology of plants (Ecol- Roger Orellana. Biologist, Facul- gación Científica de Yucatán, Professor, University of Cali- ogy). Centro de Investigación tad de Ciencias, UNAM, Mexico. fornia Riverside. USA. Científica de Yucatán, México. México. MSc Biology, Facul-

364 0378-1844/06/05/364-07 $ 3.00/0 MAY 2006, VOL. 31 Nº 5 RESUMO

Realizaram-se observações em um lote (milpa) abandonado colonização foi maior em ambos locais durante a etapa de de oito anos de idade e em uma selva madura para determinar chuvas, esta porcentagem foi igual de elevada em uma tempo- a dinâmica estacional e a recuperação de uma perturbação na rada de secas na milpa abandonada. A densidade de esporas associação micorrízica arbuscular (MA) presente em Desmon- foi maior na temporada de secas. Os valores calculados de cus orthacanthos Martius. Em uma prova em invernadeiro se RMD se encontram entre 7.8 e 54.9%, com uma maior avaliou a dependência micorrízica relativa (RMD) desta espé- biomassa nas plantas micorrizadas comparadas com as não- cie. No campo se selecionaram quatro etapas de crescimento micorrizadas usando concentrações de fósforo similares às pre- nesta palmeira e se monitorou durante um ano as raízes e o sentes no solo dos locais de estudo. Os resultados sugerem que solo rizosférico de cinco indivíduos de cada etapa de cresci- esta espécie é dependente da associação micorrízica nas condi- mento. Detectou-se uma dinâmica estacional, mas não difere ções avaliadas e mantêm uma atividade de AM relativamente na atividade da associação comparando a milpa abandonada e alta inclusive durante a temporada de seca. Os resultados tam- a selva madura. Não se encontrou correlação, durante o perío- bém sugerem que as práticas agrícolas empregadas na zona de do de estudo, entre a umidade do solo, densidade de esporas estudo permitem a recuperação do potencial de inóculo do por grama de solo e colonização de raízes. A porcentagem de solo para o crescimento de D. orthacanthos.

portance of the mycorrhizal orthacanthos Martius in the orthacanthos can association in tropical eco- southern part of the Yucatan dominate the systems, there is relatively Peninsula (Mexico). This canopy in some little basic information on the species grows in the under- secondary forests, role of this association in story of seasonal tropical for- and is recognized such a diverse and complex est in mature as well as sec- by the production system (Janos, 1980a; Huante ondary forest. It is harvested of infructescences et al., 1993), as well as a by local people to produce composed of red lack of knowledge of the handcrafts, so it has commer- berries that mature mycorrhizal fungal life cycle cial value and could be in- from July to Sep- and their capacity to track cluded in reforestation ef- tember, and are changes in edaphic and mi- forts. AM fungi have been probably dispersed croclimatic conditions observed in the roots of this by birds. Juveniles Figure 1. Ombrothermic diagram of long term (Brundrett, 2002). species (Carrillo et al., are frequently mean monthly temperature and monthly precipita- In tropical systems, studies 2002), but their function has found at low den- tion at study area. Data from the nearest observa- of seasonal root colonization not been examined. As part sities in mature tory (modified from Orellana et al., 1999a). or density of spores in soil of a program to understand forests; but by (e.g, Johnson and Wedin, the ecology and horticulture contrast, their densities are with the rainy season from 1997; Guadarrama and Álva- of this species (Orellana et higher in disturbed areas May through October. An- rez-Sánchez, 1999; Picone, al., 1999b), a study was initi- such as abandoned croplands, nual mean temperature 2000) are scarce, and even ated to observe the dynamics even though predation and varies from 24 to 26ºC, fewer studies have evaluated of AM root colonization and sapling mortality may be in- and precipitation is 1200- these for the long term spore production of D. tense. Biological and eco- 1500mm (Figure 1). Soils in (Allen et al., 1998, 2003). It orthacanthos in mature and logical studies of this species this area originated from is important to evaluate tem- secondary forest, and to test are scarce (Orellana et al., calcareous materials, and poral and disturbance dynam- its dependency on AM in 1999b; Siebert, 2000). rendzins, vertisols, luvisols ics of the mycorrhizal asso- greenhouse conditions. Carrillo et al. (2002) found and gleysols dominate. The ciation since the seasonality AM associations in roots of original vegetation is ever- of host plants and their re- Methods individuals occurring in both green to semi evergreen sponse to the symbiosis are disturbed and undisturbed ar- tropical forest with 20-30m related to their strategy for Species of study eas. Their roots were de- canopy heights. Plants were nutrient uptake and competi- scribed as Magnolioid type, sampled in mature forest tion (Bethlenfalvay, 1992). Desmoncus orthacanthos is as originally classified by and abandoned cropland, Nevertheless, these dynamics a Neotropical, scandent Baylis (1975). where soil chemical param- are poorly understood, and it Arecaceae that is broadly eters are different (Table I). is difficult to make predic- used for the production of Study area The populations of D. ortha- tions about the importance furniture and handcrafts by canthos present in the two and response of plants to farmers in regions that were Field observations and sites had different plant mycorrhizae (Bethlenfalvay, originally covered with ever- sampling were carried out at structure in terms of age 1992; Sanders and Fitter, green and semi-evergreen the ejido (communal farm- distribution and size. 1992). tropical forests from southern land) of Noh-Bec, located in The purpose of this study Mexico to and the central-southern portion Mature forest. The mature was to determine the sea- (Henderson et al., 1995). of Quintana Roo State, forest site is located at sonal patterns and recovery People who use this palm Mexico, between 19º02'30'' 19º07'28''N and 88º20'25''W. from disturbance by arbuscu- species prefer to harvest ma- to 19º12'30''N and 88º13' It is a semi-evergreen mature lar mycorrhizal (AM) asso- ture individuals with stems 30''W to 88º27'30''W. The forest that, according to some ciations in Desmoncus more than 30m in length. D. climate is warm sub-humid elder inhabitants, was not

MAY 2006, VOL. 31 Nº 5 365 TABLE I sodium hexametaphospate). Statistical analyses CHEMICAL CHARACTERISTICS OF SOILS FROM Spores contained in the sus- FOREST AND ABANDONED MILPA pension were collected and All field data were square- Soil parameters Mature Abandoned filtered over a 45µm pore pa- root transformed to ensure forest milpa per. Only whole spores were equality of variance and nor- Extractable phosphorous (mg·kg-1 soil) 18.8 13.5 counted and spore density mality. One-way analysis of Total nitrogen (cmol·kg-1 soil) 67.8 16.9 was expressed as a number variance for repeated meas- Organic matter (%) 5.2 3.3 of spores per gram of dry urements (ANOVA-RM) was et al. pH 7.3 7.1 soil. used (Kleinbaum , 1998) to compare root colonization Mycorrhizal dependency and spore density in different disturbed for 80 years or months both sites (mature of D. orthacanthos sampling dates; one-way more. The canopy was forest and abandoned milpa) ANOVA was used to compare 20-30m tall, dominated by were sampled and survival of Seeds of D. orthacanthos the same parameters between Pouteria unilocularis (Engel) individuals was recorded; in were collected in both forest growth stages for each obser- Eyma, Alseis yucatanensis case an individual died it and abandoned milpa, and vation date; and Student's t- Standl., Metopium brownei was replaced by the nearest were germinated in humid tests were used to compare (Jacq.) Urban, with the un- palm at the same growth chambers using sterilized differences among stages and derstory palms Cryosophila stage. Roots and rhizosphere vermiculite as substrate. Af- between sites. In addition, stauracantha (Heynh.) R. soil were collected from la- ter 10 days of germination, Pearson’s correlation test was Evans and Sabal mauritiifor- belled individuals to a depth one seedling was transplanted used to evaluate relationships mis (H. Wendl. Ex- H. of 20cm, selecting roots per pot, and each pot was between root colonization, Karst.) Griseb. and H. Wendl. ≤2mm in diameter. Roots filled with 350ml of steril- spore density and soil mois- were rinsed and fixed in a ized vermiculite. In the my- ture. Abandoned milpa (cornfield). 70:29:1 (volumetric) water: corrhizal treatment 100ml of The abandoned milpa site is ethanol:glycerine solution. At soil from the forest (36 Results located at 19º05'54''N and least 250ml of rhizosphere propagules: colonized roots, 88º13'30''W. This area was soil were collected from ev- spores and extraradical hy- Survival covered with early secondary ery individual and air dried. phae of arbuscular mycor- vegetation; originally it was Soil moisture was determined rhizal fungi per 100ml soil) Except for juveniles, which used for traditional maize gravimetrically. was applied. Non-mycor- had 60% and 80% survivals slash and burn agriculture to rhizal treatments were inocu- in mature forest and aban- grow corn for 2 years (8-10 Laboratory methods lated with 100ml of pasteur- doned milpa, D. orthacanthos years before present field ized forest soil to eliminate had a survival of 100% in all work was initiated). The Root samples were mycorrhizal propagules. To stages of growth, one year of dominant tree species were bleached in 10% KOH and recover the natural soil observation. The decreased

Cecropia peltata L., Bursera H2O2 and stained with trypan microbiota in the non-mycor- survival of juveniles may simaruba (L.) Sarg., Gua- blue (Phillips and Hayman, rhizal treatment, 100ml of have been from and stem zuma ulmifolia Lam. and 1970). From each sample, 10 soil filtrate using Whatman predation observed in the Guettarda combsii Urb., with fragments of 1cm were ran- 42 filter paper was applied field. a canopy of 10-15m. domly selected, and mycor- according to Azcón-Aguilar rhizal root colonization was and Barea (1996). AM structures Field methods determined by microscope Pots were randomly dis- observations (40×). For each tributed in a greenhouse. Six AM fungal structures were In March 2001, 5 individu- sample, 75 microscopic fields treatments were applied: found in all root observations. als of D. orthacanthos from (1mm diameter) were exam- three levels of P concentra- The most common structures 4 previously defined growth ined and counted as colo- tion (4, 12 and 24ppm) avail- observed were intraradical hy- stages were selected and la- nized when hyphae, vesicles able for plants in the sub- phae inside the cortical tissue, belled in each site. Growth or arbuscules were observed strate, and two mycorrhizal but hyphal coils, vesicles and stages were determined as- (McGonigle et al., 1990). levels (mycorrhizal and non- internal spores were also ob- suming a relationship be- Colonization % was calcu- mycorrhizal). Each treatment served, and in few cases tween height and develop- lated as the ratio of the num- had six replicates. Every 15 small arbuscules. The AM ment stage (Orellana et al., ber of colonized sections and days 100ml of Hoagland’s colonization was originally 1999b). Individuals 35-50cm total number of fragments nutrient solution was applied recognized as Paris type. in height were considered ju- analyzed. to the pots, using KH2PO4 Only % total colonization is veniles (J); individuals 50- AM fungal spore density (1M) to adjust the P level re- reported, as structures other 120cm were considered sap- in rhizosphere soil was esti- quired. Relative mycorrhizal than internal hyphae were lings (S); those with height mated by a modified deter- dependency of D. orthacan- sparse (<5% of observations). >120cm and without signs of gent-sucrose flotation method thos was calculated according reproduction were considered (Allen et al., 1979): soils to Plenchette et al. (1983) as Patterns of root colonization immature adults (A); and were air-dried and sieved to RMD= [(mean dry weight of those >120cm with visible <2mm; from each soil mycorrhizal plants – mean Roots of D. orthacanthos signs of reproductive struc- sample 1g was centrifuged in dry weight of non-mycor- had AM fungal colonization tures (inflorescence or fruit) water and then suspended in rhizal plants) / mean dry at all sampling dates. The were considered mature detergent-sucrose solution weight of non-mycorrhizal values ranged from 5 to 33% adults (M). Every 3 to 4 (720mg/ml sucrose, 10mg/ml plants] × 100. for individuals in the mature

366 MAY 2006, VOL. 31 Nº 5 Figure 2. Average ±SE of root colonization in D. orthacanthos from mature forest (a) and abandoned milpa (b). Bars marked with different letters are significantly different (p<0.05). n= 5.

Figure 3. Average ±SE of spores per gram of soil from rhizosphere of D. forest, while colonized indi- tween the two field sites orthacanthos from mature forest (a) and abandoned milpa (b). Bars marked viduals from the abandoned (t=2.97, p<0.02) on one with different letters are significantly different (p<0.05). n= 5. milpa varied from 6 to 34%. date only (March 2001), Higher values of root coloni- and only at the mature adult zation were observed in Sep- stage. Mature adults from mature forest showed sea- p<0.05), but not on any other tember for all stages in the the abandoned milpa had sonal variation (F=16.9, date. Immature adult palms mature forest (Figure 2a). In higher root colonization p<0.0001; Figure 3a). Sea- also showed differences in the abandoned milpa the (34.4%) than mature adults sonality was also observed September (t=2.97, p<0.02) highest values of root coloni- from the mature forest when different growth stages but not on other dates (Fig- zation were observed in (5.4%; Figure 2a, b). were analyzed separately. ure 3a, b). March 2001 and also in Sep- Spore density patterns in the tember for all stages (Figure Spore density abandoned milpa showed the Correlation between root 2b). Overall AM root coloni- same dynamics as those ob- colonization, spores and soil zation in mature forest Spores of AM fungi were served in mature forest, with moisture (F=19.8, p<0.001) and in observed in rhizosphere soils significant differences in abandoned milpa (F=14.3, on all dates and growth spore density among sam- Using Pearson's correla- p<0.001) showed seasonal stages. The density of spores pling dates (F=12.2, tion test, there is no signifi- dynamics for all growth from mature forest was p<0.0001). Separate analyses cant correlation (p>0.05 in stages, except for saplings in higher in both March 2001 for different stages showed both sites and juveniles in and 2002 than at the other no significant differences be- abandoned milpa. sampling dates. In the aban- tween sample dates for sap- In general there were no doned milpa, this tendency lings (S) in the abandoned significant differences in % toward higher spore density milpa, but there was seasonal root colonization among in March was only observed variation in spore density for growth stages within a sample in samples from juveniles all other growth stages. date at either the mature for- (J) and mature palms (M; Spore density was higher est or abandoned milpa. One Figure 3a, b). Spore density in juvenile palms in aban- exception occurred in aban- of AM fungi from the rhizo- doned milpa than mature for- doned milpa in June 2001, sphere of individuals in the est in September (t=2.84, when juveniles (J) had signifi- cantly lower % colonization TABLE II than immature adults (A) AVERAGE ±SE OF TOTAL DRY WEIGHT OF D. orthacan- (F=3.36, p<0.05). There were thos GROWING AT THREE AVAILABLE P LEVELS no significant differences Dry weight (g) among stages in any sample 4ppm P 12ppm P 24ppm P dates in spore density at ei- Mycorrhizal plants 1.24 ±0.14 0.55 ±0.12 0.51 ±0.12 Figure 4. Relative mycorrhizal de- ther site (p>0.05 in all cases). Non-mycorrhizal plants 0.73 ±0.18 0.44 ±0.11 0.47 ±0.12 pendency of D. orthacanthos calcu- Root colonization was lated according to Plenchette et al. significantly different be- (n= 6) (1983). n= 6.

MAY 2006, VOL. 31 Nº 5 367 all cases) between the values stages, indicating that my- is also the flowering season 2003). Arbuscules are not of either spore density or % corrhizal inoculum was not for D. orthacanthos, a time the only structure for trans- colonization and soil mois- the major limiting factor for when other researchers have porting nutrients, and ture, and between root colo- establishment (unpublished reported higher than normal vesicles and intraradical hy- nization and spore density. data). % colonization (Corkidi and phae, which were observed Both AM fungal activity and In another study that ex- Rincón, 1997) so high colo- in D. orthacanthos, are indi- soil moisture showed sea- amined mycorrhizal inocu- nization could be an indica- cators of current and past sonal dynamics, but these lum following slash and tor of high effort of growth colonization (Allen, 1991). did not track each other burning in Quintana Roo, and development, however Furthermore, arbuscules are closely. Fungal activity was the percentage of coloniza- there are also contrasting re- ephemeral structures that de- maintained during the dry tion was comparable to ma- ports (Koide and Dickie, grade after 3-7 days (Toth season, often with no sig- ture forest within a year, 2002). and Miller, 1984; Tester et nificant reduction compared and the AM spore species The studies that have re- al., 1987; Mohammad et al., to the rainy season. composition recovered ported seasonality of the 1998). Anyway in this spe- within 4 years after the fire mycorrhizal association gen- cies Paris colonization type Mycorrhizal dependency of (Allen et al., 2003). Leaf erally assume a direct influ- were observed and small D. orthacanthos and stem predation, most ence of environmental con- arbuscules may be difficult likely by insects (Siebert, ditions such as temperature to observe, but it is probable A positive effect of AM 2000; J. Ramos-Zapata, per- and moisture on the fungi that both Paris and Arum inoculation on the produc- sonal communication) was (Sigüenza et al., 1996; Mo- types may be present, as re- tion of dry weight (DW) for probably the cause of mor- hammad et al., 1998; Nehl ported by Dickson (2004). the D. orthacanthos seed- tality of the juvenile stage. et al., 1998). In fact, the Seasonality of spore pro- lings was observed. The Thus, there is no direct rela- percentage of root coloniza- duction has been observed in highest DW in the seedlings tionship between % coloni- tion may decrease during the wet tropics (Guadarrama and was found in the treatment zation and survival of juve- rainy season if there is a Álvarez-Sánchez, 1999) and with 4ppm of P. The treat- niles at the abandoned milpa high rate of root production seasonal tropics (Allen et ment with AM inoculation and forest sites. In fact, later (Allen, 2001). Conversely, al., 1998, 2003). The results also showed higher values growth stages had no higher during drought there may be from D. orthacanthos show than the non-inoculated colonization than juveniles, high values of root coloniza- a higher density of spores treatment (Table II). The either. Instead, it is more tion due to a slow rate of during the dry season relative mycorrhizal depen- useful to understand the sea- root growth (Koide and (March of both years) than dency was greatest for the sonal dynamics of AM as an Mooney, 1987; Cade-Menun the rainy season, indicating plants that received the low- important factor for the es- et al., 1990). In the present that spore production was est level of P, but there was tablishment and growth of study, soil moisture was re- inversely related to soil a positive biomass response this species. lated to root production; moisture. This inverse rela- to all three levels of added Mycorrhizal fungi usually samples from June 2001 and tionship has also been ob- P (Figure 4). track seasonal soil moisture March 2002 had a high den- served in other studies on changes quite closely, espe- sity of fine new roots, even seasonality of spore produc- Discussion cially in seasonal climates though June is in the rainy tion (Douds and Millner, such as seasonally dry tropi- season and March is in the 1999; Miller and Bever, Many reports indicate that cal forest (Allen et al., dry season; both of these 1999). The density of spores the development of a mycor- 1998, 2003). The results of times had reduced % coloni- was in the same range of rhizal association plays an this study on D. orthacan- zation. In fact, multiple fac- values as other studies in important role in improving thos were surprising in that tors are likely responsible tropical and seasonal tropi- establishment of seedlings in the relationships between for the percentage of coloni- cal forest (Johnson and a competitive system, such both % root colonization zation, including environ- Wedin, 1997; Allen et al., as a tropical forest (Gange and spore density were not mental conditions, rate of 1998, 2003; Picone, 2000) et al., 1993; Francis and significantly correlated with root vs fungal growth, phe- although higher than wet Read, 1994; Lovera and soil moisture, and there nology and physiological tropical forest (Guadarrama Cuenca, 1996; Pedersen and were still active roots with status of the plant (De Mars and Álvarez-Sánchez, 1999). Sylvia, 1996; Zobel et al., relatively high % coloniza- and Boerner, 1995; Allen, An absence of differences 1997). The reduced survivor- tion during the dry season. 2001; Brundrett, 2002). in the mycorrhizal associa- ship of juveniles in both the This may indicate that this The presence of tion between a mature forest mature forest (60%) and the species is dependent on my- arbuscules is often consid- and abandoned cultivated abandoned milpa (80%) in- corrhizae during the entire ered the best indicator of field could be explained in dicate that this is the limit- year; in fact % colonization functioning in the AM asso- terms of sufficient time for ing stage for successful es- in the abandoned milpa dur- ciation (Tester et al., 1987; recovery (successional stage), tablishment of the species ing the height of the dry McGonigle et al., 1990; since the latter was aban- (e.g. Escalante et al., 2004). season in March 2001 was Corkidi and Rincón, 1997; doned 8 to 10 years ago, and The values of root coloniza- as high as in the following Gange and Ayres, 1999), but secondary vegetation has tion by AM fungi in juve- September, at the middle of arbuscules were found only colonized the area. Further- niles were not different in the rainy season, as has in about 1% of the observa- more, slash and burn agricul- the abandoned milpa and been found for other palm tions. This was also the case ture maintains high levels of mature forest, nor was colo- species in a tropical forest for other tree and herb spe- soil inoculum (Allen et al., nization different in general (Núñez-Castillo and Álvarez- cies of seasonal tropical for- 2003). The ability of juve- among the four growth Sánchez, 2003). September est (Allen et al., 1998, niles to form a mycorrhizal

368 MAY 2006, VOL. 31 Nº 5 association similar to older to high P levels are normal et al., 2003), so this palm versity Press. Cambridge, UK. stages may be promoted by and high levels of coloniza- maintains an active root sys- 184 pp. the high soil inoculum. The tion also occur (Allen et al., tem when others become dor- Allen MF (2001) Modeling arbus- AM association likely influ- 2003). mant. Flower and fruit pro- cular mycorrhizal infection: is % infection an appropriated ences the fitness of this spe- The pot experiment also duction of D. orthacanthos variable? Mycorrhiza 10: 255- cies at all growth stages. did not simulate drought occur during the wet season, 258. Individuals of D. orthacan- stress that may occur in the when AM fungi may be im- Allen MF, Moore TS, Christensen thos showed mycorrhizal de- field during the dry season. portant to maintain growth, JRM, Stanton N (1979) pendency, even at high avail- Soil moisture was still nearly but AM fungi may be impor- Growth of vesicular-arbuscular- able P concentration in the 40% in these highly organic tant to reduce drought stress mycorrhizal and non-mycor- rhizal Bouteloua gracilis in a solution. The response of soils for plants sampled at the and promote hydraulic lift defined medium. Mycologia tropical plants to mycorrhizae dry season. These values of during the dry season (Quere- 71: 666-669. ranges from facultative to ob- soil moisture are high consid- jeta et al., 2003). Amijee F, Tinker P, Stribley V ligate, depending on the suc- ering that there had been vir- Mycorrhizae in tropical (1989) The development of cessional stage, size of seed, tually no rain for 2-3 months palms have received relatively endomycorrhizal root systems. and nutrient requirements at the March sample dates. little attention (Fisher and VII. A detailed study of effects of soil phosphorus on coloni- (Janos, 1980b; Huante et al., One hypothesis that could ex- Jayachandran, 1999). An un- zation. New Phytol. 111: 435- 1993; Siqueira et al., 1998; plain high soil moisture dur- derstanding of the mycor- 446. Sharma et al., 2001; Siqueira ing dry periods is the hydrau- rhizal relationships of D. or- Attiwill P, Adams M (1993) Nutri- and Saggin-Junior, 2001; lic lift from areas of higher thacanthos can contribute to ent cycling in forest. New Phy- Allen et al., 2003). The RMD soil water, such as deeper soil its conservation and, given its tol. 124: 561-582. value and the presence of layers, to the soil surface high potential (Orellana et al., Augé RM (2001) Water relations, magnolioid roots in this spe- where plants deplete soil 1999b; Siebert 2000; Esca- drought and vesicular-arbuscu- cies (Baylis, 1975) suggest moisture. Mycorrhizal fungi lante et al., 2004), enable cul- lar mycorrhizal symbiosis. My- corrhiza 11: 3-42. that, according to Janos are especially important in tivation for economic pur- Azcón-Aguilar C, Barea J (1996) (1980a), D. orthacanthos may promoting hydraulic lift, as poses. The fact that mycor- Arbuscular mycorrhizas and be an obligate mycorrhizal the surfaces of extramatrical rhizal colonization was biological control of soil-borne plant in the semi-evergreen hyphae act as a capillary con- equally high in the abandoned plant pathogens-an overview of tropical forest of Quintana duit (Querejeta et al., 2003). milpa and the mature forest the mechanisms involved. My- Roo, Mexico. D. orthacanthos maintains indicates that the indigenous corrhiza 6: 457-464. Gemma et al. (2002) mycorrhizal colonization dur- practice of slash and burn ag- Baylis GTS (1975) The magnoloide mycorrhiza and mycotrophy in pointed out that the “ecologi- ing the dry season. This re- riculture maintains a healthy root systems derived from it. cal mycorrhizal dependency” cent discovery of the impor- soil inoculum, and is congru- In Sanders F, Mosse B, Tinker can be evaluated if the experi- tance of the extramatrical hy- ent with initiating a plantation P (Eds.) Endomycorrhizas. ments to calculate dependency phae in promoting hydraulic program for a species such as Academic Press. London, UK. are carried out at the same P lift further explains the impor- D. orthacanthos that has my- pp. 373-389. substrate concentrations as in tance to plants in maintaining corrhizal dependency. Bethlenfalvay GJ (1992) Mycor- rhizae in the agricultural plant- the field where the plants a mycorrhizal association dur- soil system. Symbiosis 14: grow in normal conditions. ing the dry season. D. ortha- ACKNOWLENDGEMENTS 413-425. The values of 12 and 24ppm canthos may be an obligatory Bhatia NV, Sundari K, Adholeya A correspond to values found in mycorrhizal dependent in or- The authors thank Lilia (1996) Diversity and selective field soils, and promoted a der to survive and maintain Carrillo and Roberto Sibaja dominance of vesicular-arbus- mycorrhizal growth response. physiological activity during cular mycorrhizal fungi. In for helping in field and labo- Mukerji KG (Ed.) Concepts in Of course, the greenhouse the dry season. Further physi- ratory work. JRZ received a Mycorrhizal Research. Kluwer. growth conditions did not ological studies of this spe- doctoral grant (153737) from Dordrecht, Netherland. pp. simulate field conditions, es- cies in the field are required. the Consejo Nacional de 133-178. pecially as an artificial growth D. orthacanthos produced Ciencia y Tecnología (CONA- Brundrett MC (2002) Co-evolution medium was used so that low new fine roots during both CYT), Mexico. of roots and mycorrhizas of P conditions could be tested. the wet and the dry season, land plants. New Phytol. 154: We are not aware of the oc- and the % AM colonization 275-304. currence of natural soils in of D. orthacanthos was high REFERENCES Cade-Menun B, Berch S, Bomke A (1990) Seasonal colonization the region with the low P of during both seasons. 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