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Animal-Mediated Organic Matter Transformation: Aquatic Insects As a Source of Microbially Bioavailable Organic Nutrients and Energy

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Animal-Mediated Organic Matter Transformation: Aquatic Insects As a Source of Microbially Bioavailable Organic Nutrients and Energy Received: 11 June 2018 ( Accepted: 30 October 2018 DOI: 10.1111/1365-2435.13242 !"#"$!%&'$!()%*" !"#$%&'$()#%*()+,-.%"#/+$%**(-+*-%"01,-$%*#,"2+!34%*#/+ #"0(/*0+%0+%+0,4-/(+,1+$#/-,5#%&&6+5#,%7%#&%5&(+,-.%"#/+"4*-#("*0+ %")+("(-.6 Thomas B. Parr8 ( Krista A. Capps9:; ( Shreeram P. Inamdar8 ( Kari A. Metcalf< #Q*>,-16*310540R:,310,390D52:0 D.2*3.*B0S32T*-+2180540Q*:,U,-*B0V*U,-=B0 !50*-%/* Q*:,U,-* 1. Animal communities are essential drivers of energy and elemental flow in ecosys< ! Odum School of Ecology, University of 1*6+'0X5U*T*-B04*U0+1792*+0/,T*023T*+12;,1*901/*0473.1253,:0-5:*0540,326,:+0,+0 Georgia, Athens, Georgia sources of dissolved organic matter (DOM) and the subsequent utilization of that 3Savannah River Ecology Laboratory, Aiken, D571/0W,-5:23, DOM by the microbial community. CTetra Tech Inc, Portland, Maine 2. In a small forested headwater stream, we tested the effects of taxonomy, feeding Correspondence traits, and body size on the quality and quantity of dissolved organic carbon (DOC) J/56,+0N'0R,-- and dissolved organic nitrogen (DON) excreted by aquatic insects. In addition, we Email: [email protected] .5397.1*90+1*,98<+1,1*0+5:71*0,9921253+0150*+126,1*023+1-*,609*6,39045-0:,?2:*0W0 Present Address ,390.56>,-*902101501/*0W0*M.-*1*90?8023T*-1*?-,1*+' J/56,+0N'0R,--B0Q*>,-16*310540N25:5;8B0 Oklahoma Biological Survey, University of 3. Individual excretion rates and excretion composition varied with body size, tax< Oklahoma, Norman, Oklahoma 535680,3904**923;0;72:9'0J/*0*+126,1*90,T*-,;*0.566732180*M.-*12530-,1*0U,+0 −1 −1 −1 <# 1.31 μg DOC· per mg insect dry weight (DW) 0/- and 0.33 μg DON·mg DW 0/- B0 =4")#".+#"1,-$%*#," + University of Delaware, Grant/Award and individuals excreted DON at nearly twice the rate of NH4 . Number: IIA-1301765; University of 4. This DOM was 2–5 times more bioavailable to microbial heterotrophs than ambi< Oklahoma, Grant/Award Number: DEB- 1457542 ent stream water DOM. 5. We estimated that the insect community, conservatively, excreted 1.62 mg of bio< Handling Editor: Shawn Leroux available DOC·m−20/-−10,3901/-57;/0+1*,98<+1,1*0,9921253+06*,+7-*90,30,6?2*310 labile C demand as 3.97 ± 0.67 mg C m−20/-−1'0J/2+0+7;;*+1+01/,1023+*.1<6*92,1*90 transformation and excretion of labile DOC could satisfy a significant fraction (40 ± 7%) of labile C demand in this small stream. O'0 W5::*.12T*:8B057-0-*+7:1+0+7;;*+101/,10,326,:0*M.-*12530>:,8+0,30*++*312,:0473.1253,:0 -5:*02301-,3+45-623;05-;,32.06,11*-02315062.-5?2,::80?25,T,2:,?:*045-6+0,3906,80 +,12+480,0T,-2,?:*0?710+2;3242.,310>5-1253054062.-5?2,:09*6,39045-0:,?2:*0W0,390V' KEYWORDS ?25;*5./*62.,:0.8.:23;B0?-5U3045590U*?B0.53+76*-0371-2*310983,62.+B092++5:T*905-;,32.0 .,-?53B092++5:T*905-;,32.0321-5;*3B062.-5?2,:0*.5+8+1*6B05-;,32.06,11*-09*.56>5+21253 1 ( INTRODUCTION ?25;*5./*62.,:0.8.:*+0@A*1.,:4*0*10,:'B0!"#C%0D./621E0*10,:'B0!"#C%0 F,3;0 G0 H-,1153B0 !"#C%0 I57B0 J/K?,7:1B0 L,.-52MB0 G0 N,-51B0 !"#OP'0 )*+*,-./0,101/*0231*-4,.*0540.566732180,390*.5+8+1*60*.5:5;8023< J/*0,?739,3.*B0?256,++B0,390473.1253,:0,3901,M53562.0.56>5< .-*,+23;:80+**=+0150739*-+1,3901/*0473.1253,:0-5:*0,326,:+0>:,80230 +21253+0540,326,:0.56673212*+0.,30+/,>*01/*0+152./256*1-8B0-,1*+0 !"#$%&'#()*+$')',-.*!"#$%#&#!' wileyonlinelibrary.com/journal/fec !"#$%&"'()"*+,(-./0"1+23,4-256"73-6-89" ( ! !"#$%&":.4,4/("73-6-84356";-34),9 2 " Functional Ecology !"##$%&$"'( ,3906,;32179*+0540*:*6*31,:04:5U+01/-57;/0*.5+8+1*6+0T2,0.53< inorganic nutrient recycling. As such, animal influences on inor< +76*-<9-2T*30371-2*310.8.:23;B0U/2./0.,3B023017-3B0234:7*3.*045590 ;,32.0371-2*310.8.:23;0,-*065-*0*44*.12T*:80231*;-,1*9023150?25;*5< web dynamics (Atkinson, Capps, Rugenski, & Vanni, 2017; Roman ./*62.,:0,39045590U*?0659*:+01/,30,-*0,326,:<6*92,1*9026>,.1+0 & McCarthy, 2010; Vanni, 2002). Inorganic nutrient recycling on organic nutrient dynamics and the flow of energy (Atkinson 23*M1-2.,?:80:23=+01/*01-5>/2.0983,62.+0540;-**305-0>-26,-80>-5< et al., 2017; Zou et al., 2016). Though limited, evidence suggests 97.1253<?,+*9045590U*?+0U21/01/5+*0540?-5U305-09*1-217+<?,+*90 that a portion of ingested resources are excreted as DOC (James, 45590U*?+0@Q,74-*+3*B0L,.-52MB0N*3/,26B0G0L5-*,7B0!""$%0R,.*B0 Xenopoulos, Wilson, & Frost, 2007; Meyer & O’Hop, 1983), which Cole, Carpenter, & Kitchell, 1999; Zou et al., 2016). In contrast, 6,80 ?*0 :*410 65-*0 ?25,T,2:,?:*0 97*0 150 >/8+2.,:0 @*';'B0 4-,;6*31,< 1/*06,;32179*0540,326,:<6*92,1*904:5U+05405-;,32.0371-2*31+0,390 1253P0 ,390 ./*62.,:0 @*3E86,12.0 ?-*,=95U30 540 6,.-565:*.7:*+P0 5-;,32.0*3*-;80,3901/*0473.1253,:0-5:*+01/*+*0>:,80230*.5+8+1*6< digestive processes (Jumars et al., 1989; Metcalfe et al., 2014; level processes are understudied. Importantly, animal metabolism Moore et al., 2004). In a detritus-based ecosystem, addition of 6*92,1*+0 1/*0 5315;*32.0 1-,3+45-6,12530 540 45590 -*+57-.*+B0 >-5< labile carbon stimulated microbial production and subsequently 97.23;0>,-12.7:,1*0,39092++5:T*905-;,32.0U,+1*+0@W/*-240G0L5-*,7B0 enhanced detritivore production (Wilcox, Bruce Wallace, Meyer, 2013; Jumars, Penry, Baross, Perry, & Frost, 1989; Moore et al., & Benstead, 2005). Thus, microbes utilizing labile organic excreta !""CPY1/*0:,11*-0540U/2./06,80+7>>5-1047-1/*-062.-5?2,:0>-597.< ,3904-560,326,:+04**923;02301/*0;-**305-0?-5U3045590U*?+06,80 tion (Jumars et al., 1989; Nagata, 2000). Thus, organic “wastes” >-5T29*0,0>5+212T*04**9?,.=0530,326,:+04**923;0530?-5U3045590 >-597.*90?80,326,:+06,80-*>-*+*310,0+2;3242.,310?25;*5./*62.,:0 U*?062.-5?*+' 4:7M0540:,?2:*05-;,32.06,11*-01/,1047-1/*-0:23=+0;-**30,390?-5U30 S39*-+1,3923;01/*0-5:*+054023+*.1+0230>-597.23;062.-5?2,::80 45590U*?+' ?25,T,2:,?:*0 *3*-;80 ,390 371-2*31+0 4-560 5-;,32.0 6,11*-0 2+0 26< Insects are key detritivores in many ecosystems and, after mi< >5-1,31045-0>-*92.123;0/5U0?25;*5./*62.,:0>-5.*++*+0,39045590 crobes, are often the most ubiquitous and abundant animals and crit< U*?0 983,62.+0 -*+>5390 150 ,31/-5>5;*32.0 >*-17-?,1253+0 1/,10 ical drivers of ecosystem function (Yang & Gratton, 2014). In streams, negatively impact insect abundance (Hallmann et al., 2017) and insects process large quantities of living and detrital organic matter, 92T*-+2180 @Q2-E50 *10 ,:'B0 !"#CPB0 ,390 1/,10 >-597.*0 +/241+0 230 23+*.10 and accelerate decomposition (Wallace & Webster, 1996). The use of .566732180.56>5+212530@X,U=23+0G0F7,3B0!"#OP'0J502::7623,1*0 9244*-*31045590-*+57-.*+09*>*39+B0230>,-1B0530,302392T297,:Z+04**923;0 the role of animals in shaping the quantity, chemical composi< guild (functional feeding group (FFG; Cross, Wallace, & Rosemond, tion and bioavailability of DOM in streams, we focused on in< 2007). For instance, shredders (vascular plant tissues and some mi< sects and asked two questions: (a) How do taxonomy and trophic .-5?*+P0 ,390 >-*9,15-+0 @.53+7623;0 51/*-0 ,326,:+P0 /,T*0 92+123.10 -*< feeding guilds affect the rate and composition of DOM excreted +57-.*0?,+*+B0U/2:*0.5::*.15-+0@;,1/*-*-+0,39042:1*-*-+P0,390+.-,>*-+0 by aquatic insects? (b) Does DOM excreted by insects provide an share a resource base (microbes, algae and detritus). Some aquatic energy and/or nutrient subsidy to heterotrophic microbes? We insects can satisfy >20% and up to 100% of their C demands by con< investigated these questions through field excretion incubations suming bacteria (Collins, Sparks, Thomas, Wheatley, & Flecker, 2016; measuring the rate and composition of DOM excretion, and lab< Hall & Meyer, 1998). 5-,15-80*M>*-26*31+06*,+7-23;01/*062.-5?2,:09*;-,9,1253054023< Growth of microbial heterotrophs (hereafter “microbes”) may sect-excreted DOM. ?*0:2621*905-0.5<:2621*90?805-;,32.0*3*-;80@:,?2:*0WP05-0371-2*310@VB0 P) availability (Daufresne et al., 2008; Sinsabaugh, Hill, & Follstad Shah, 2009). Much of this resource demand is supplied by dissolved 2 ( MATERIALS AND METHODS organic matter (DOM; Jumars et al., 1989; Meyer, 1994)—a complex 62M17-*054065:*.7:*+0U21/0*:*6*31,:0+152./256*1-2*+095623,1*90?80 The Fair Hill Experimental Watershed (39.718° N, 75.835° W) is C, H, O, N, P and S. In marine and freshwater ecosystems, <20% ,0U*::<+1792*90.:5+*<.,35>2*90/*,9U,1*-0+1-*,60U,1*-+/*90U21/0 of the ambient DOC is typically bioavailable to heterotrophic mi< 42-+1<0,390+*.539<5-9*-0+7?U,1*-+/*9+02301/*0V5-1/*-30R2*965310 crobes (Søndergaard & Middelboe, 1995), most likely leaving them ecoregion of Maryland, United States of America. The mean an< .,-?53<:2621*905-0.,-?53<371-2*31+0.5<:2621*90@N*-3/,-910G0L2=*3+B0 nual water temperature is 12.6°C and ranges from 0°C during the 2002; Daufresne et al., 2008; Sinsabaugh, Follstad Shah, Hill, & winter to 24°C (S.
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