Next Article in Journal
Impact of Sowing Time on Chickpea (Cicer arietinum L.) Biomass Accumulation and Yield
Previous Article in Journal
Spring Precipitation Deficiency in Poland and Its Temporal and Spatial Variability in the Context of Agricultural Needs
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Communication

Stem Carbon Dioxide Efflux of Lignophytes Exceeds That of Cycads and Arborescent Monocots

Western Pacific Tropical Research Center, University of Guam, Mangilao, GU 96923, USA
Agronomy 2022, 12(1), 159; https://doi.org/10.3390/agronomy12010159
Submission received: 6 November 2021 / Revised: 3 January 2022 / Accepted: 7 January 2022 / Published: 10 January 2022
(This article belongs to the Section Horticultural and Floricultural Crops)

Abstract

:
Tree stem CO2 efflux (Es) can be substantial and the factors controlling ecosystem-level Es are required to fully understand the carbon cycle and construct models that predict atmospheric CO2 dynamics. The majority of Es studies used woody lignophyte trees as the model species. Applying these lignophyte data to represent all tree forms can be inaccurate. The Es of 318 arborescent species was quantified in a common garden setting and the results were sorted into four stem growth forms: cycads, palms, monocot trees that were not palms, and woody lignophyte trees. The woody trees were comprised of gymnosperm and eudicot species. The Es did not differ among the cycads, palms, and non-palm monocots. Lignophyte trees exhibited Es that was 40% greater than that of the other stem growth forms. The Es of lignophyte gymnosperm trees was similar to that of lignophyte eudicot trees. This extensive species survey indicates that the Es from lignophyte tree species do not align with the Es from other tree growth forms. Use of Es estimates from the literature can be inaccurate for understanding the carbon cycle in tropical forests, which contain numerous non-lignophyte tree species.

1. Introduction

The efflux of carbon dioxide (CO2) from tree stem surfaces (Es) has been extensively studied to answer various questions and more fully understand the global carbon cycle [1,2]. As with many aspects of biology research, the Es literature is biased toward one subset of biodiversity. Most case studies of tree Es have focused exclusively on lignophyte species with stems comprised mostly of wood constructed by true bifacial secondary cambium. This expansive literature contains only a few examples in which pachycaulous tree species with stems devoid of bifacial secondary cambium were represented [3,4,5,6].
A major contributor to Es is stem tissue respiration. However, numerous interacting factors coalesce to define Es in space and time. For example, CO2 from root respiration can be transported to stems by way of xylem, and this CO2 can exit xylem within stems to increase the Es above that of stem tissue respiration [7,8]. This transported CO2 is under the influence of diel variations in sap flow [9,10]. The movement of CO2 from the internal tissues to stem surfaces can also be under the control of temporal storage or re-fixation [11]. These and other interacting factors can cause the Es to be heavily influenced by CO2 that was respired from tissues that are distant from the site of efflux [12].
A recent study designed to understand the diel patterns of Es for arborescent cycads, monocots, and lignophytes [6] included only six species of each growth form. Other studies that compared different stem tissue anatomy and its influence in Es were restricted to lignophyte species [13,14,15]. An extensive survey to compare the Es of trees with disparate stem growth forms has not been conducted to date in a single forest or garden. I hypothesized that Es from an extensive range of tree species would sort into significantly different groups, based on stem design. The objective of this study was to use the large living collection in a common garden setting to compare the Es of four growth forms used to design and construct tree stems.

2. Materials and Methods

This study was conducted at Nong Nooch Tropical Botanical Garden in Sattahip, Thailand. The location and characteristics of this living collection have been described [6]. The dates of measurements were 8–15 July 2019. In this setting and this time of year, the Es of non-lignophyte trees was not influenced by the time of day, but the lignophyte trees exhibited greater Es during midday [6]. Therefore, the measurements for this extensive species survey were restricted to the hours of 900–1500 h on each day of measurement.
A total of 99 cycad species were included (Table A1). There were 96 lignophyte species included (Table A2). The arborescent monocot species were separated into two groups. A total of 17 arborescent monocot taxa that were not palm species were included (Table A3). Finally, there were 106 palm species in the study (Table A4).
The Es was measured, as previously described [4,5,6]. Vigorous trees with no obvious wounds or decay on the stems were selected. A CIRAS EGM-4 analyzer fitted with a SRC-1 close system chamber (PP Systems, Amesbury, MA, USA) was used to quantify the Es from the stem surfaces. The chamber was secured using modeling clay as the sealant at a stem height of 30–40 cm above the root collar. The EGM-4 recorded the air temperature, and the chamber’s increase in CO2 concentration above ambient was quantified after a 2 min period. The change in CO2 concentration was used to calculate the flux by dividing by area and time. Three periods of efflux were recorded at different radial locations for each sampling period for each tree.
The stem surface temperature was measured with an infrared thermometer (Milwaukee Model 2267-20, Milwaukee Tool, Brookfield, WI, USA). The relative humidity was determined with a sling psychrometer every hour during the periods of measurements. The stem diameter at the height of measurements and total stem height were measured for each tree.
Two sampling periods were applied to each species. For taxa with more than one large tree, this included two trees. For taxa with a single large tree, the two samples were from the same tree but separated by at least three days. The data were sorted according to four stem growth forms: cycad species, palm species, arborescent non-palm monocot species, and lignophyte species. The data were subjected to ANOVA using the PROC MIXED model (SAS Institute, Cary, NC, USA) with unequal replications. There were 636 observations in the data set, two per species. The two observations were treated as subsamples in the analysis. The means separation was conducted by Tukey’s HSD test.

3. Results and Discussion

The cycad trees were represented by 53 Cycadaceae and 46 Zamiaceae species (Table A1). The stem circumference ranged from 51–169 cm with a mean of 96 cm. The mean stem temperature was 31.8 °C and the concomitant mean air temperature was 32.6 °C. Individual Es measurements ranged from 0.5–6.2 µmol·m−2·s−1. The lignophyte trees were represented by 34 families (Table A2). The stem circumference ranged from 51–156 cm with a mean of 84 cm. The mean stem temperature was 31.3 °C and concomitant mean air temperature was 32.0 °C. Individual Es measurements ranged from 0.2–7.6 µmol·m−2·s−1. The monocot trees that were not palm species were represented by five families (Table A3). The stem circumference ranged from 51–175 cm with a mean of 82 cm. The mean stem temperature was 31.5 °C and the concomitant mean air temperature was 32.1 °C. The individual Es measurements range from 0.8–4.7 µmol·m−2·s−1. The palm species representing the Arecaceae family exhibited a stem circumference ranging from 48–182 cm with a mean of 71 cm (Table A4). The mean stem temperature was 31.7 °C and the concomitant mean air temperature was 32.4 °C. The individual Es measurements ranged from 0.7–7.5 µmol·m−2·s−1. The relative humidity ranged from 56% to 69% and did not change substantially among the hours and dates of the study.
The stem CO2 efflux differed among the four stem growth forms (F3,314 = 10.64, p < 0.001). The means separated into two groups, with the lignophyte species exhibiting greater Es than the other three stem growth forms (Table 1). The lignophyte trees exhibited Es that was 40% greater than the mean of the other growth forms. No differences in the Es occurred among the cycad, palm, and non-palm monocot stem forms.
Cycads and monocot trees often produce thick primary growth constructed by a primary thickening meristem, and do not possess bifacial secondary cambium to increase stem diameter at distances away from the stem tip [16,17,18,19,20,21,22]. For all of these trees, the peripheral tissues are ground tissue with vascular tissues embedded closer to the stem center. One of the factors that influences CO2 efflux from a stem surface is the diffusion and conductance constraints imposed by tissues that are peripheral to tissues that serve as the greatest internal source of CO2, such as sap flow in xylem [23]. The substantial radial distance of xylem tissues and other major sources of CO2 from the stem surface of these pachycaulous trees can account for the greater mean Es for lignophyte trees, which has been shown herein.
Considering the prominence of these pachycaulous trees in tropical forests, the historical exclusion of them from Es studies is unfortunate. Indeed, the CO2 derived from stem efflux can represent up to 40% of the CO2 contributed to by vegetation [1,24]. This survey, represented by 222 pachycaulous tree species, confirms the earlier findings based on a limited number of species [6], and indicates that attempts to use the Es literature based on the lignophyte species can over-estimate the Es in regions that are represented by these tree species.
Cycads comprise the most threatened contemporary plant group [25]. Conservation physiology has emerged as a critical component of the suite of conservation strategies, because an understanding of the physiological responses of threatened organisms to their escalating biotic and abiotic threats is required for successful species recovery [26,27]. For federally listed endangered cycad species in the United States, such as Cycas micronesica K.D. Hill (see Table A1), understanding the physiology of the taxa is crucial for developing effective federal recovery plans [28]. Clearly, the pursuit of more cycad physiology studies will advance the nascent discipline of conservation physiology.
Future research on the Es of cycad and monocot trees will be required to fully understand the reasons that mean Es is less than the mean Es of lignophyte trees. The design of cycad stems is fairly homogeneous, with vascular cylinders inserted between the persistent living pith and cortex [29]. The design of palm stems is also fairly homogeneous with vascular bundles scattered through the ground tissue [19,22]. However, the design of the non-palm arborescent monocot tree stems is heterogeneous among the families. A closer look at this group of pachycaulous species can yield interesting findings about what endogenous factors mostly control the Es of these non-lignophyte trees.
In conclusion, the many factors that interact to control the magnitude of CO2 efflux from tree stem surfaces are differentially expressed among various tree stem designs. The results herein suggest that the traits of stem peripheral tissues can be among the defining factors that cause the differences in Es among various tree growth forms.

Funding

This research was partly funded by the United States Forest Service, grant numbers 17-DG-11052021-217.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data is available in the Appendix.

Acknowledgments

I thank Nong Nooch Tropical Botanical Garden for the logistical support and access to the living collection. I thank Dallas Johnson for the statistical analysis.

Conflicts of Interest

The author declares no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Appendix A

Table A1. List of cycad species included in the carbon dioxide efflux study. Circ = circumference, Air T = air temperature, and Stem T = surface temperature of stems.
Table A1. List of cycad species included in the carbon dioxide efflux study. Circ = circumference, Air T = air temperature, and Stem T = surface temperature of stems.
SpeciesFamilyCirc (cm)Air TStem TSample 1Sample 2
Ceratozamia delucana Vázq.Torres, A.Moretti and Carvajal-Hern.Zamiaceae843232.92.62222.3290
Ceratozamia latifolia Miq.Zamiaceae723132.92.32272.0197
Ceratozamia robusta Miq.Zamiaceae1123133.12.25011.9566
Cycas angulata R.Br.Cycadaceae1073232.85.77455.1166
Cycas apoa K.D.HillCycadaceae763332.54.86334.2288
Cycas badensis K.D.HillCycadaceae823231.11.75121.5148
Cycas beddomei DyerCycadaceae783331.71.78191.5508
Cycas bougainvilleana K.D.HillCycadaceae653231.14.15223.6103
Cycas cairnsiana F.Muell.Cycadaceae1013131.42.07491.8051
Cycas campestris K.D.HillCycadaceae933230.42.44422.1251
Cycas chamaoensis K.D.HillCycadaceae1013231.81.84631.5969
Cycas changjiangensis N.LiuCycadaceae813331.71.02252.2722
Cycas clivicola K.D.HillCycadaceae873331.72.03771.7805
Cycas couttsiana K.D.HillCycadaceae953332.10.90891.1361
Cycas curranii (J.Schust.) K.D.HillCycadaceae1033230.15.14934.4800
Cycas debaoensis Y.C.Zhong and C.J.ChenCycadaceae1103230.91.52031.3191
Cycas diannanensis Z.T.Guan and G.D.TaoCycadaceae843332.15.66784.9231
Cycas edentata de Laub.Cycadaceae683229.81.92121.6663
Cycas elongata (Leandri) D.Y.WangCycadaceae1033231.92.14601.7042
Cycas falcata K.D.HillCycadaceae893331.82.84031.4517
Cycas furfuracea W.Fitzg.Cycadaceae1083434.52.55642.2217
Cycas glauca Miq.Cycadaceae923332.24.00453.5346
Cycas hainanensis C.J.Chen ex C.Y.Cheng, W.C.Cheng and L.K.FuCycadaceae913331.42.54962.2217
Cycas hongheensis S.Y.Yang and S.L.YangCycadaceae823230.82.28472.1165
Cycas inermis Lour.Cycadaceae1093332.16.19345.4154
Cycas javana (Miq.) de Laub.Cycadaceae1123332.72.79452.4300
Cycas macrocarpa Griff.Cycadaceae753131.24.11643.6103
Cycas media R.Br.Cycadaceae823331.92.19641.8996
Cycas megacarpa K.D.HillCycadaceae623331.82.11141.8380
Cycas micronesica K.D.HillCycadaceae623332.51.37641.1992
Cycas nathorstii J.Schust.Cycadaceae1023231.91.74461.5148
Cycas nongnoochiae K.D.HillCycadaceae883331.92.95132.5689
Cycas ophiolitica K.D.HillCycadaceae1153332.11.18461.0225
Cycas pachypoda K.D.HillCycadaceae983230.84.41123.8482
Cycas papuana F.Muell.Cycadaceae863130.75.33124.6517
Cycas pectinata Buch.-Ham.Cycadaceae933233.42.05471.7805
Cycas petrae A.Lindstr. and K.D.HillCycadaceae693332.11.79652.3353
Cycas platyphylla K.D.HillCycadaceae1163331.70.68171.5905
Cycas pranburiensis Yang, Tang, Hill and VatcharakornCycadaceae783332.51.51151.3210
Cycas revoluta Thunb.Cycadaceae853232.82.22231.9314
Cycas riuminiana Porte ex RegelCycadaceae653333.13.77843.2821
Cycas rumphii Miq.Cycadaceae843032.14.05613.5346
Cycas seemannii A.Br.Cycadaceae633231.13.02962.1523
Cycas semota K.D.HillCycadaceae843330.23.48653.0296
Cycas shanyaensis G.A.FuCycadaceae683232.12.46903.0296
Cycas siamensis Miq.Cycadaceae793231.93.44312.9867
Cycas silvestris K.D.HillCycadaceae693332.21.66791.4517
Cycas sphaerica Roxb.Cycadaceae923230.43.41552.9867
Cycas taitungensis Shen, Hill, Tsou and ChenCycadaceae833231.84.44783.8880
Cycas tansachana K.D.Hill and S.L.YangCycadaceae1133331.81.18641.0099
Cycas thouarsii R.Br.Cycadaceae823130.91.19681.0225
Cycas tropophylla K.D.Hill and P.K.LôcCycadaceae943332.12.03121.7673
Cycas tuckeri K.D.HillCycadaceae953230.81.71571.4933
Cycas wadei Merr.Cycadaceae833231.32.11131.8380
Cycas yorkiana K.D.HillCycadaceae943332.12.15641.8746
Cycas zeylanica (J.Schust.) A.Lindstr. and K.D.HillCycadaceae783330.82.33122.0103
Dioon argenteum Gregory, Chemnick, Salas-Morales and VovidesZamiaceae933331.14.94554.4308
Dioon caputoi De Luca, Sabato and Vázq.TorresZamiaceae913234.82.48572.1523
Dioon edule Lindl.Zamiaceae1553233.13.77953.2821
Dioon mejiae Standl. and L.O. WilliamsZamiaceae983331.61.95941.7042
Dioon merolae De Luca, Sabato and Vázq.TorresZamiaceae1103232.74.91324.2920
Dioon spinulosum Dyer ex Eichl.Zamiaceae913332.22.25611.9566
Encephalartos aemulans VorsterZamiaceae1383331.94.44663.9976
Encephalartos altensteinii Lehm.Zamiaceae1163432.22.25042.4679
Encephalartos arenarius R.A.DyerZamiaceae973332.21.44951.5905
Encephalartos bubalinus MelvilleZamiaceae1253331.71.05691.1614
Encephalartos chimanimaniensis R.A.Dyer and I.Verd.Zamiaceae1213331.81.59481.7420
Encephalartos concinnus R.A.Dyer and VerdoornZamiaceae1143332.14.97655.4465
Encephalartos dyerianus Lavranos and D.L.GoodeZamiaceae1243432.93.50043.8501
Encephalartos equatorialis P.J.H.HurterZamiaceae1273432.91.77641.9314
Encephalartos eugene-maraisii Verd.Zamiaceae1163332.12.24652.4679
Encephalartos inopinus R.A.DyerZamiaceae1213432.22.36112.5878
Encephalartos lebomboensis I.Verd.Zamiaceae973332.31.65641.8146
Encephalartos mackenziei L.E.NewtonZamiaceae1113332.20.86450.9089
Encephalartos macrostrobilus S.Jones and WyantsZamiaceae1253432.81.79461.9566
Encephalartos manikensis (Gilliland) GillilandZamiaceae1333331.71.59461.7420
Encephalartos msinganus VorsterZamiaceae1083332.12.97643.2663
Encephalartos munchii R.A.Dyer and I.Verd.Zamiaceae1343332.22.33312.5562
Encephalartos natalensis R.A.Dyer and I.Verd.Zamiaceae1093432.91.19151.3065
Encephalartos paucidentatus Stapf and Burtt DavyZamiaceae1203332.51.77641.9314
Encephalartos princeps R.A.DyerZamiaceae1133332.82.06451.8947
Encephalartos pterogonus R.A.Dyer and I.Verd.Zamiaceae1193333.12.44652.6986
Encephalartos sclavoi De Luca, D.W.Stev. and A.MorettiZamiaceae1013332.11.59591.7420
Encephalartos senticosus VorsterZamiaceae1073230.90.84650.8710
Encephalartos septentrionalis Schweinf.Zamiaceae1193432.91.66943.7239
Encephalartos tegulaneus MelvilleZamiaceae1243332.13.69154.0647
Encephalartos transvenosus Stapf and Burtt DavyZamiaceae1283331.24.51214.9357
Encephalartos whitelockii P.J.H.HurterZamiaceae1633231.12.71542.9865
Lepidozamia hopei (W.Hill) RegelZamiaceae643229.11.48961.2623
Lepodozamia peroffskyana RegelZamiaceae923233.81.67651.8304
Macrozamia moorei F.Muell.Zamiaceae1693232.71.86861.6663
Microcycas calocoma (Miq.) A.DC.Zamiaceae913232.12.06441.8304
Zamia elegantissima Schutzman, Vovides and R.S.AdamsZamiaceae513330.91.33121.4517
Zamia furfuracea L.f.Zamiaceae913332.11.71541.8746
Zamia gentryi DodsonZamiaceae633330.52.01052.1999
Zamia imperialis A.S.Taylor, J.L.Haynes and HolzmanZamiaceae593231.11.38661.5148
Zamia lindenii Regel ex AndréZamiaceae783029.92.01662.1998
Zamia obliqua A.BraunZamiaceae513230.22.76262.9965
Zamia skinneri Warsc.Zamiaceae583230.22.34652.5765
Table A2. List of the lignophyte species included in the carbon dioxide efflux study. Circ = circumference, Air T = air temperature, and Stem T = surface temperature of stems.
Table A2. List of the lignophyte species included in the carbon dioxide efflux study. Circ = circumference, Air T = air temperature, and Stem T = surface temperature of stems.
SpeciesFamilyCirc (cm)Air TStem TSample 1Sample 2
Acacia auriculiformis A.Cunn. Ex Benth.Fabaceae923229.33.55663.7944
Adansonia digitata L.Malvaceae713131.43.94653.5346
Adansonia madagascariensis Baill.Malvaceae693332.32.05661.8304
Afrocarpus gracilior (Pilg.) C.N. PagePodocarpaceae723231.36.44656.3748
Agathis dammara (Lamb.) Rich.Araucariaceae853332.22.34652.5698
Agathis moorei (Lind.) Mast.Araucariaceae523330.91.32551.8304
Agathis robusta (C.Moore ex F.Muell.) BaileyAraucariaceae553230.91.71981.8935
Albizia saman (Jacq.) Merr.Fabaceae1563230.61.27651.3886
Amherstia nobilis Wall.Fabaceae683231.42.18941.9566
Annona squamosa L.Annonaceae623130.81.67681.8746
Araucaria bidwillii Hook.Araucariaceae913231.25.00324.4813
Araucaria columnaris J.R.Forst. HookAraucariaceae693030.26.22645.6237
Araucaria cunninghamii MudieAraucariaceae583129.42.36312.0829
Araucaria heterophylla (Salisb.) FrancoAraucariaceae963233.22.84032.7771
Araucaria luxurians (Brongn. and Grisb.) de Laub.Araucariaceae643130.16.00215.4281
Araucaria montana Brong. and GrisAraucariaceae543231.82.90342.6643
Araucaria nemorosa de Laub.Araucariaceae933331.82.08292.0197
Artocarpus altilis (Parkinson) FosbergMoraceae883332.13.66253.9986
Artocarpus heterophyllus Lam.Moraceae743130.82.46892.7140
Averrhoa bilimbi L.Oxalidaceae723332.34.21654.6647
Averrhoa carambola L.Oxalidaceae693130.14.44653.9865
Bougainvillea sp. Comm. Ex Juss.Nyctaginaceae513332.11.99552.1133
Brachychiton acerifolius (A.Cunn ex G.Don) F.Muell.Malvaceae533131.72.25662.0134
Brachychiton rupestris (T.Mitch. Ex Lindl.) K.Schum.Malvaceae543030.34.46564.0269
Bursera simaruba (L.) Sarg.Burseraceae513230.80.81190.9026
Callistemon viminalis (Sol. Ex Gaertn.) G.DonMyrtaceae773030.76.00225.4154
Callistris baileyi C.T. WhiteCupressaceae593130.82.66442.3984
Calophyllum sil Lauterb.Clusiaceae1033030.93.31863.0107
Cananga odorata (Lam.) Hook.f. and ThomsonAnnonaceae1213231.14.42124.8766
Casuarina equisitifolia L.Casuarinaceae1023333.43.55643.8965
Cavanillesia hylogeiton Ulbr.Malvaceae1113332.82.88452.5562
Cecropia obtusifolia Bertol.Urticaceae883130.35.11144.6012
Cecropia peltata L.Urticaceae1133231.63.62663.2265
Ceiba pentandra (L.) Gaertn.Malvaceae1233331.94.34893.9196
Clusia rosea Jacq.Clusiaceae613331.33.11533.5642
Delonix decaryi (R.Vig.) CapuronFabaceae823231.71.33491.1992
Delonix regia (Hook.) Raf.Fabaceae723231.23.66443.2947
Dimocarpus longan Lour.Sapindaceae1263332.32.88442.5649
Diospyros discolor Willd.Ebenaceae1293331.70.51160.4418
Diospyros nigra (J.F.Gmel.) PerrierEbenaceae993028.94.14454.5444
Elaeocarpus hygrophilus KurzElaeocarpaceae533130.83.97873.5699
Euphorbia kamponii Rauh and PetignatEuphorbiaceae533333.21.18991.3065
Euphorbia laeta AitonEuphorbiaceae813433.54.80114.2920
Fernandoa madagascariensis (Baker) A.H.GentryBignoniaceae513130.32.06451.8304
Ficus benjamina L.Moraceae1513029.83.22332.9034
Ficus elastica Roxb. ex Hornem.Moraceae943332.23.61513.2663
Ficus lyrata Warb.Moraceae1043231.46.11845.8793
Ficus natalensis Hochst.Moraceae563129.85.61125.0083
Garcinia cymosa (K.Schum.) I.M.Turner and P.F.StevensClusiaceae643231.33.23112.9760
Guaiacum officinale L.Zygophyllaceae743230.54.33653.8956
Inga edulis Mart.Fabaceae643332.21.08480.9650
Kopsia arborea BlumeApocynaceae783130.81.13230.9976
Lagerstroemia indica L.Lythraceae663331.95.71125.1125
Lagerstroemia speciosa (L.) Pers.Lythraceae783332.16.30545.6616
Leucaena leucocephala (Lam.) de WitFabaceae513230.82.02022.2091
Litsea elliptica BlumeLauraceae623231.32.11321.8935
Magnolia × alba (D.C.) FiglarMagnoliaceae1453231.81.66501.5148
Mallotus barbatus Müll.Arg.Euphorbiaceae823030.35.77655.1347
Mangifera foetida Lour.Anacardiaceae573333.47.49866.9429
Mangifera indica L.Anacardiaceae613333.54.00653.5847
Melaleuca bracteata F. Muell.Myrtaceae963130.21.00651.4466
Morinda citrifolia L.Rubiaceae613030.71.33891.4678
Moringa hildebrandtii Eng.Moringaceae823231.24.11323.6608
Moringa oleifera Lam.Moringaceae753332.10.22110.1894
Muntingia calabura L.Muntingiaceae663231.11.56441.3886
Nephelium lappaceum L.Sapindaceae1283332.31.86861.6663
Nerium oleander L. Apocynaceae523230.81.22341.1321
Pachira aquatica Aub.Malvaceae1053332.12.00441.7988
Pachira insignis (Sw.) SavignyMalvaceae953030.65.21235.8068
Persea americana Mill.Lauraceae1263332.51.55901.3232
Phyllanthus acidus (L.) SkeelsPhyllanthaceae863231.11.43911.5565
Pithecellobium dulce (Roxb.) Benth.Fabaceae963231.81.62651.4517
Plumeria rubra L.Apocynaceae733331.65.37955.9764
Podocarpus neriifolius D.DonPodocarpaceae853029.84.30354.7965
Polyalthia longifolia (Sonn.) ThwaitesAnnonaceae933332.13.11382.7105
Pouteria campechiana (Kunth.) BaehniSapotaceae1383230.71.11332.0197
Pseudobombax septenatum (Jacq.) DugandMalvaceae663130.70.99220.8836
Psidium guajava L.Myrtaceae523030.84.95975.5416
Robinia hispida L.Fabaceae663331.82.44652.2247
Sandoricum koetjape (Burm.f.) Merr.Meliaceae1413332.11.93221.7042
Saraca asoca (Roxb.) Willd.Fabaceae723130.34.16454.5679
Saraca declinata Miq.Fabaceae753230.13.01113.3452
Saraca thaipingensis PrainFabaceae893130.71.09461.1992
Schizolobium parahyba (Vll.) S.F.BlakeFabaceae913231.10.99550.8836
Senegalia polyacantha (Willd.) Siegler and EbingerFabaceae813331.83.79894.2265
Sterculia foetida L.Malvaceae1413332.43.48443.8877
Syzygium cumini (L.) SkeelsMyrtaceae1513230.24.60753.9764
Syzygium forte (F.Muell.) B.HylandMyrtaceae1133131.51.21341.3255
Syzygium malaccense (L.) Merr. and L.M.PerryMyrtaceae913331.82.22332.4616
Tamarindus indica L.Fabaceae1193332.26.66447.5740
Tecoma stans Griseb.Bignoniaceae613331.92.16452.3984
Tectona grandis L.f.Lamiaceae653332.20.65660.6943
Terminalia catappa L.Combretaceae533030.52.48442.7771
Terminalia ivorensis A.Chev.Combretaceae693331.93.54673.9865
Triplaris americana L.Polygonaceae973231.12.55462.8403
Xanthostemon chrysanthus (F.Muell.) Benth.Xanthorrhoeaceae963332.23.61344.0395
Table A3. List of non-palm arborescent monocot species included the in carbon dioxide efflux study. Circ = circumference, Air T = air temperature, and Stem T = surface temperature of stems.
Table A3. List of non-palm arborescent monocot species included the in carbon dioxide efflux study. Circ = circumference, Air T = air temperature, and Stem T = surface temperature of stems.
SpeciesFamilyCirc (cm)Air TStem TSample 1Sample 2
Beaucarnea recurvata Lem.Asparagaceae843130.23.18482.8466
Dasylirion wheeleri S.Watson ex Rothr.Asparagaceae993332.64.44894.0032
Dracaena cochinchinensis (Lour.) S.C.ChenAsparagaceae1173231.52.94412.6509
Dracaena dereminis Engl.Asparagaceae583332.51.22341.0730
Dracaena floribunda BakerAsparagaceae1013332.22.04981.8304
Dracaena fragrans (L.) Ker Gaw.Asparagaceae663332.13.48993.0927
Ensete ventricosum (Welw.) CheesmanMusaceae1753331.84.70034.2099
Musa x paradisiaca L.Musaceae753130.52.44682.6798
Pandanus dubius Spreng.Pandanaceae733231.73.55643.9888
Pandanus rabaiensis Rendle.Pandanaceae643332.13.91663.4714
Pandanus tectorius Parkinson ex Du RoiPandanaceae713131.23.08653.4470
Pandanus utilis BoryPandanaceae583231.80.76580.8205
Pandanus vandermeeschii Balf.f.Pandanaceae683130.33.84654.2920
Pandanus veitchii Mast.Pandanaceae723332.22.17792.3984
Ravenala madagascariensis Sonn.Strelitziaceae853130.61.00440.9468
Strelitzia alba (L.f.) SkeelsStrelitziaceae513231.13.56684.0547
Xanthorrhoea glauca D.J.BedfordXanthorrhoeaceae783131.51.44651.5779
Table A4. List of the Arecaceae species included in the carbon dioxide efflux study. Circ = circumference, Air T = air temperature, and Stem T = surface temperature of stems.
Table A4. List of the Arecaceae species included in the carbon dioxide efflux study. Circ = circumference, Air T = air temperature, and Stem T = surface temperature of stems.
SpeciesCirc (cm)Air TStem TSample 1Sample 2
Adonia merrillii (Becc.) Becc.663331.91.48681.3255
Aiphanes minima (Gaertn.) Burret533331.83.36223.6797
Allagoptera caudescens (Mart.) Kuntze523230.81.66231.8051
Archontophoenix myolensis Dowe873132.82.44652.1460
Archontophoenix purpurea Hodel and Dowe513231.24.16573.6645
Areca catechu L.593231.81.81652.0134
Areca macrocarpa Becc.613332.13.77994.3046
Areca parens Becc.593333.93.21363.5649
Astrocaryum mexicanum Leibm. Ex Mart.513231.12.56442.2722
Beccariophoenix alfredii Rakotoarin., Ranariv. and J.Dransf.1823332.91.11650.9864
Beccariophoenix madagascariensis Jum. and H.Perrier1033231.23.66454.0031
Bentinckia nicobarica (Kurz.) Becc.653231.83.16193.4466
Borassodendron machadonis Becc.1273331.22.86453.1165
Brassiophoenix schumannii (Becc.) Essig523332.11.71151.5274
Burretiokentia dumasii Pintaud and Hodel513231.12.76543.0031
Burretiokentia grandiflora Pintaud and Hodel523231.74.29584.7799
Burretiokentia vieillardii (Brongn. and Gris) Pic.Serm.513331.90.82860.8898
Calyptrocalyx spicatus (Lam.) Blume523432.91.29891.1361
Calyptronoma rivalis (O.F.Cook) L.H.Bailey663331.72.67982.9765
Carpentaria acuminata (H.Wendl. and Drude) Becc.523332.22.27221.7042
Carpoxylon macrospermum H.Wendl. and Drude673230.90.93460.9979
Caryota ophiopellis Dowe813231.13.99664.9643
Chambeyronia macrocarpa (Brongn.) Vieill. Ex Becc.513332.11.88791.6410
Chelyocarpus chuco (Mart.) H.E.Moore513231.13.66264.0033
Chelyocarpus ulei Dammer513331.84.74745.2646
Clinostigma ponapense (Becc.) H.E.Moore and Fosberg623332.13.62643.9986
Clinostigma samoense H.Wendl.683331.84.89465.3970
Cocos nucifera L.1053231.43.77644.1133
Colpothrinax wrightii Griseb. and H.Wendl. ex Voss1013332.21.84451.6474
Copernicia baileyana León1623231.50.96310.9987
Copernicia hospita Mart.613130.33.08443.4125
Copernicia prunifera (Mill.) H.E.Moore643332.14.94975.4895
Copernicia sp. Mart. ex Endl.683231.61.33461.4653
Corypha utan Lam.1053332.13.08883.4102
Cryosophila warscewiczii (H.Wendl.) Bartlett613331.94.00543.6103
Cryosophila williamsii P.H.Allen523231.15.49865.0896
Cyphophoenix elegans (Brongn. and Gris) H.Wendl. ex Salomon513332.12.72982.3755
Cyphophoenix nucele H.E.Moore523231.63.19593.0296
Cyrtostachys elegans Burret583231.14.11213.6570
Cyrtostachys loriae Becc.523332.13.16452.8165
Dictyosperma album (Bory) Scheff.583231.31.38961.2497
Dypsis arenarum (Jum.) Beentje and J.Dransf.633433.15.11324.5547
Dypsis cabadae (H.E.Moore) Beentje and J.Dransf.523332.73.31322.9765
Dypsis carlsmithii J.Dransf. and Marcus773332.94.60024.1165
Dypsis decaryi (Jum.) Beentje and J.Dransf.813231.23.44973.1133
Dypsis hovomantsina Beentje623333.71.38863.1349
Dypsis ifanadianae Beentje583333.14.15463.8845
Dypsis lastelliana (Baill.) Beentje and J.Dransf.773333.26.11325.6068
Dypsis madagascariensis (Becc.) Beentje and J.Dransf.553433.55.77465.1770
Dypsis mananjarensis (Jum. and H.Perrier) Beentje and J.Dransf.653431.93.84653.4545
Dypsis montana (Jum.) Beentje and J.Dransf.653332.24.00643.6699
Dypsis pembana (H.E.Moore) Beentje and J.Dransf.682928.14.59594.2236
Dypsis plumosa Hodel, J.Marcus and J.Dransf.623231.51.99762.8965
Dypsis robusta Hodel, Marcus and J.Dransf.693433.91.84651.6410
Dypsis saintelucei Beentje553433.11.92921.7042
Elaeis guineensis Jacq.1183332.21.16451.0235
Euterpe precatoria Mart.513231.42.42652.1775
Heterospathe elata Scheff.643332.12.31642.1050
Heterospathe intermedia (Becc.) Fernando513231.24.34653.9133
Heterospathe sibuyanensis Becc.743431.92.00651.8304
Hydriastele moluccana (Becc.) W.J.Baker and Loo843433.13.88443.4466
Hyophorbe lagenicaulis (L.H.Bailey) H.E.Moore1513130.42.88972.5878
Itaya amicorum H.E.Moore553230.92.42462.1460
Kentiopsis piersoniorum Pintaud and Hodel553332.11.44651.3255
Kentiopsis pyriformis Pintaud and Hodel653231.23.66113.2821
Laccospadix australasicus H.Wendl. and Drude513332.71.79961.5969
Licuala bayana Saw513230.82.11321.8935
Licuala peltata Roxb.583231.31.00540.8836
Licuala sallehana Saw693029.11.66321.5148
Livistona lanuginosa Rodd973332.12.82772.5247
Livistona mariae F.Muell.883332.31.13120.9957
Livistona muelleri F.M.Bailey743231.51.84861.6410
Livistona victoriae Rodd793130.91.66451.5148
Lodoicea maldivica (J.F.Gmel.) Pers.983434.61.11320.9720
Medemia argun (Mart.) Wurttenb. ex H.Wendl.1173230.32.79182.5878
Neonicholsonia watsonii Drammer523230.81.77651.5148
Neoveitchia brunnea Dowe553331.82.00211.8051
Neoveitchia storckii (H.Wendl.) Becc.733231.21.23451.1109
Nephrosperma van-houtteanum (H.Wendl. ex Van Houtte) Balf.f.523332.32.77112.4657
Oenocarpus mapora H.Karst513231.15.50564.9231
Orania moluccana Becc.682928.61.64651.4391
Pelagodoxa henryana Becc.673231.31.42151.6410
Phoenix sylvestris (L.) Roxb.1093132.93.71644.1132
Pinanga batanensis Becc.683432.93.61344.0066
Pinanga insignis Becc.483331.92.03111.8304
Pinanga javana Blume513432.82.17981.9566
Pinanga urosperma Becc.613331.90.95540.8205
Ponapea hosinoi Kaneh.623331.85.41656.0023
Prestoea acuminata (Willd.) H.E.Moore523230.84.01544.4651
Pritchardia thurstonii F.Muell. and Drude662928.60.78790.6943
Ptychosperma elegans (R.Br.) Blume533231.26.38977.1322
Ravenea madagascariensis Becc.523433.20.94981.1021
Rhopaloblaste augusta (Kurz.) H.E.Mllre583332.21.63551.4517
Rhopaloblaste ceramica (Miq.) Burret723231.11.68991.5148
Sabal mauritiiformis (H.Karst.) Griseb. and H.Wendl.713231.43.11343.2265
Sabal palmetto (Walter) Lodd. ex Schult. and Schult.f.953131.31.34441.2231
Saribus rotundifolius (Lam.) Blume1053030.11.13141.0099
Satakentia liukiuensis (Hatus.) H.E.Moore683231.57.51096.3365
Schippia concolor Burret513332.40.75440.7547
Syagrus botryophora (Mart.) Mart.763232.61.76551.5779
Syagrus romanzoffiana (Cham.) Glassman633332.11.26151.1165
Syagrus sancona (Kunth.) H.Karst.783231.81.63111.4517
Syagrus schizophylla (Mart.) Glassman563231.11.56441.3886
Veitchia joannis H.Wendl.593332.21.34331.1992
Washingtonia robusta H.Wendl.1543231.34.68994.2288
Wodyetia bifurcata A.K.Irvine993031.64.44543.9764

References

  1. Yang, J.; He, Y.; Aubrey, D.P.; Zhuang, Q.; Teskey, R.O. Global patterns and predictors of stem CO2 efflux in forest ecosystems. Glob. Chang. Biol. 2016, 22, 1433–1444. [Google Scholar] [CrossRef] [PubMed]
  2. Vargas, R.; Barba, J. Greenhouse gas fluxes from tree stems. Trends Plant Sci. 2019, 24, 296–299. [Google Scholar] [CrossRef]
  3. Cavaleri, M.A.; Oberbauer, S.F.; Ryan, M.G. Wood CO2 efflux in a primary tropical rain forest. Global Chang. Biol. 2006, 12, 2442–2458. [Google Scholar] [CrossRef]
  4. Marler, T.E. Stem CO2 efflux of Cycas micronesica is reduced by chronic non-native insect herbivory. Plant Signal Behav. 2020, 15, 1716160. [Google Scholar] [CrossRef]
  5. Marler, T.E.; Krishnapillai, M.V. Vertical strata and stem carbon dioxide efflux in Cycas trees. Plants 2020, 9, 230. [Google Scholar] [CrossRef] [Green Version]
  6. Marler, T.E.; Lindström, A.J. Diel patterns of stem CO2 efflux vary among cycads, arborescent monocots, and woody eudicots and gymnosperms. Plant Signal Behav. 2020, 15, 1732661. [Google Scholar] [CrossRef]
  7. Bloemen, J.; McGuire, M.A.; Aubrey, D.P.; Teskey, R.O.; Steppe, K. Transport of root-respired CO2 via the transpiration stream affects aboveground carbon assimilation and CO2 efflux in trees. New Phytol. 2013, 197, 555–565. [Google Scholar] [CrossRef] [PubMed]
  8. Kunert, N. A case study on the vertical and diurnal variation of stem CO2 effluxes in an Amazonian forest tree. Trees 2018, 32, 913–917. [Google Scholar] [CrossRef]
  9. Bowman, W.P.; Barbour, M.M.; Turnbull, M.H.; Tissue, D.T.; Whitehead, D.; Griffin, K.L. Sap flow rates and sapwood density are critical factors in within- and between-tree variation in CO2 efflux from stems of mature Dacrydium cupressinum trees. New Phytol. 2005, 167, 815–828. [Google Scholar] [CrossRef]
  10. McGuire, M.A.; Cerasoli, S.; Teskey, R.O. CO2 fluxes and respiration of branch segments of sycamore (Platanus occidentalis L.) examined at different sap velocities, branch diameters, and temperatures. J. Exp. Bot. 2007, 58, 2159–2168. [Google Scholar] [CrossRef] [PubMed]
  11. Tarvainen, L.; Wallin, G.; Lim, H.; Linder, S.; Oren, R.; Ottosson Löfvenius, M.; Räntfors, M.; Tor-ngern, P.; Marshall, J. Photosynthetic refixation varies along the stem and reduces CO2 efflux in mature boreal Pinus sylvestris trees. Tree Physiol. 2018, 38, 558–569. [Google Scholar] [CrossRef]
  12. Hilman, B.; Muhr, J.; Trumbore, S.E.; Kunert, N.; Carbone, M.S.; Yuval, P.; Wright, S.J.; Moreno, G.; Pérez-Priego, O.; Migliavacca, M.; et al. Comparison of CO2 and O2 fluxes demonstrate retention of respired CO2 in tree stems from a range of tree species. Biogeosciences 2019, 16, 177–191. [Google Scholar] [CrossRef] [Green Version]
  13. Rowland, L.; da Costa, A.C.; Oliveira, A.A.; Oliveira, R.S.; Bittencourt, P.L.; Costa, P.B.; Giles, A.L.; Sosa, A.I.; Coughlin, I.; Godlee, J.L.; et al. Drought stress and tree size determine stem CO2 efflux in a tropical forest. New Phytol. 2018, 218, 1393–1405. [Google Scholar] [CrossRef] [Green Version]
  14. Salomon, R.L.; De Roo, L.; Bodé, S.; Boeckx, P.; Steppe, K. Efflux and assimilation of xylem-transported CO2 in stems and leaves of tree species with different wood anatomy. Plant Cell Environ. 2021, 44, 3494–3508. [Google Scholar] [CrossRef] [PubMed]
  15. Stutz, S.S.; Anderson, J. Inside out: Measuring the effect of wood anatomy on the efflux and assimilation of xylem-transported CO2. Plant Cell Environ. 2021, 44, 3490–3493. [Google Scholar] [CrossRef] [PubMed]
  16. Stevenson, D.W. Radial growth in Beaucarnea recurvata. Am. J. Bot. 1980, 67, 476–489. [Google Scholar] [CrossRef]
  17. Stevenson, D.W. Radial growth in the Cycadales. Am. J. Bot. 1980, 67, 465–475. [Google Scholar] [CrossRef]
  18. Stevenson, D.W.; Fisher, J.B. The developmental relationship between primary and secondary thickening growth in Cordyline (Agavaceae). Bot. Gaz. 1980, 141, 264–268. [Google Scholar] [CrossRef]
  19. Tomlinson, P.B. The Structural Biology of Palms; Clarendon Press: Oxford, UK, 1990. [Google Scholar]
  20. Rudall, P. Lateral meristems and stem thickening growth in monocotyledons. Bot. Rev. 1991, 57, 150–163. [Google Scholar] [CrossRef]
  21. Rudall, P. New records of secondary thickening in monocotyledons. IAWA J. 1995, 16, 261–268. [Google Scholar] [CrossRef] [Green Version]
  22. Tomlinson, P.B.; Huggett, B.A. Cell longevity and sustained primary growth in palm stems. Am. J. Bot. 2012, 99, 1891–1902. [Google Scholar] [CrossRef] [PubMed]
  23. Steppe, K.; Saveyn, A.; McGuire, M.A.; Lemeur, R.; Teskey, R.O. Resistance to radial CO2 diffusion contributes to between-tree variation in CO2 efflux of Populus deltoides stems. Funct. Plant Biol. 2007, 34, 785–792. [Google Scholar] [CrossRef] [PubMed]
  24. Campioli, M.; Malhi, Y.; Vicca, S.; Luyssaert, S.; Papale, D.; Peñuelas, J.; Reichstein, M.; Migliavacca, M.; Arain, M.A.; Janssens, I.A. Evaluating the convergence between eddy-covariance and biometric methods for assessing carbon budgets of forests. Nat. Commun. 2016, 7, 13717. [Google Scholar] [CrossRef]
  25. Fragniere, Y.; Bétrisey, S.; Cardinaux, L.; Stoffel, M.; Kozlowski, G. Fighting their last stand? A global analysis of the distribution and conservation status of gymnosperms. J. Biogeogr. 2015, 42, 809–820. [Google Scholar] [CrossRef]
  26. Wikelski, M.; Cooke, S.J. Conservation physiology. Trends Ecol. Evol. 2006, 21, 38–46. [Google Scholar] [CrossRef]
  27. Cooke, S.J.; O’Connor, C.M. Making conservation physiology relevant to policy makers and conservation practitioners. Conserv. Lett. 2010, 3, 159–166. [Google Scholar] [CrossRef]
  28. Mahoney, J.L.; Klug, P.E.; Reed, W.L. An assessment of the US endangered species act recovery plans: Using physiology to support conservation. Conserv. Physiol. 2018, 6, coy036. [Google Scholar] [CrossRef]
  29. Norstog, K.J.; Nicholls, T.J. The Biology of the Cycads; Cornell University Press: Ithaca, NY, USA, 1997. [Google Scholar]
Table 1. Stem carbon dioxide efflux (µmol·m−2·s−1) of arborescent species as influenced by the stem growth form.
Table 1. Stem carbon dioxide efflux (µmol·m−2·s−1) of arborescent species as influenced by the stem growth form.
Stem Growth FormnEfflux
Lignophyte 1963.421 ± 0.140 a 2
Palm1062.593 ± 0.133 b
Cycad992.415 ± 0.138 b
Monocot (non-palm)172.321 ± 0.332 b
1 The lignophyte species were eudicot and gymnosperm trees that produce true wood from secondary bifacial vascular cambium. 2 Growth form with the same letter not different according to Tukey’s HSD test.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Marler, T.E. Stem Carbon Dioxide Efflux of Lignophytes Exceeds That of Cycads and Arborescent Monocots. Agronomy 2022, 12, 159. https://doi.org/10.3390/agronomy12010159

AMA Style

Marler TE. Stem Carbon Dioxide Efflux of Lignophytes Exceeds That of Cycads and Arborescent Monocots. Agronomy. 2022; 12(1):159. https://doi.org/10.3390/agronomy12010159

Chicago/Turabian Style

Marler, Thomas E. 2022. "Stem Carbon Dioxide Efflux of Lignophytes Exceeds That of Cycads and Arborescent Monocots" Agronomy 12, no. 1: 159. https://doi.org/10.3390/agronomy12010159

APA Style

Marler, T. E. (2022). Stem Carbon Dioxide Efflux of Lignophytes Exceeds That of Cycads and Arborescent Monocots. Agronomy, 12(1), 159. https://doi.org/10.3390/agronomy12010159

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop